Normative Data for the Hayling and Brixton Tests in an Italian Population

Normative Data for the Hayling and Brixton Tests in an Italian Population Abstract Objective The Hayling and Brixton tests constitute a short test battery that quickly assesses verbal and spatial inhibition and flexibility. This battery has shown high construct validity and strong reliability in clinical and experimental settings. The aim of this study was to develop an Italian version of the Hayling and Brixton tests and obtain normative values. Method We collected normative data from 301 healthy Italian participants aged between 16 and 94 years, taking into account all demographics. To maximize the sample size, we used the overlapping interval strategy. Adjusted scores for demographics were obtained by linear regression analysis. Results The performance on the Hayling and Brixton tests was influenced by age and education. In particular, age affected verbal accuracy and response time on the Hayling Sentence Completion Test, whereas education only affected the former. Differently, the spatial component, as measured by the Brixton Spatial Anticipation Test, was shaped only by age, which decreased the number of correct responses. Conclusions Our study provides normative data that have been adjusted for relevant demographics and percentile grids in an Italian population. Our data support the use of the Hayling and Brixton tests as a valid instrument for performing neuropsychological evaluations and longitudinal analyses of executive functions in clinical practice and for research purposes. Executive functions, Hayling test, Brixton test, Neuropsychological assessment, Verbal suppression, Normative data Introduction Executive functions (EFs) refer to higher-order cognitive abilities that regulate and monitor most of our everyday actions, and they are considered to implicate a frontal–parietal network (Niendam et al., 2012) that is engaged throughout various cognitive tasks (Fedorenko, Duncan, & Kanwisher, 2013). Deficiencies in EFs occur frequently after brain damage (Azouvi et al., 2016; Bosco, Parola, Sacco, Zettin, & Angeleri, 2017; Cerezo García, Martín Plasencia, & Aladro Benito, 2015; Chung, Pollock, Campbell, Durward, & Hagen, 2013; Jelcic et al., 2013; Kennedy et al., 2008; Roman & Arnett, 2016), in psychiatric disorders (Bédard, Joyal, Godbout, & Chantal, 2009; David, Soeiro-de-Souza, Moreno, & Bio, 2014; Sharp, Miller, & Heller, 2015; Simon, Berger, Giacomini, Ferrero, & Mohr, 2006; van Beilen, van Zomeren, van den Bosch, Withaar, & Bouma, 2005; Vandborg, Hartmann, Bennedsen, Pedersen, & Thomsen, 2014; Zebdi, Goyet, Pinabiaux, & Guellaï, 2016), and in relation to aging (Mac Kay, 2016; Potter, McQuoid, Whitson, & Steffens, 2015; Turner & Spreng, 2012). Thus, for over six decades, the assessment of EFs has continued to be a significant issue. Impairments in EFs can cause deficits in response initiation and response suppression and on the rule detection task. Burgess and Shallice (1996, 1997) focused on these fundamental executive processes when they developed the Hayling and Brixton tests (HBTs). In the Hayling Sentence Completion test (HSCT), participants are asked to complete several sentences as fast as possible and required to produce or inhibit an automatic response. The response inhibition that is evoked by the HSCT is associated with increased activation of a network of left prefrontal areas (Cipolotti et al., 2016; Collette et al., 2001), and patients with executive dysfunctions perform poorly on this test (Corben et al., 2017; Dymowski, Owens, Ponsford, & Willmott, 2015; Robinson et al., 2015). The Brixton Spatial Anticipation test (BSAT; Burgess & Shallice, 1996) is a rule detection task in which participants must forecast the position of a colored stimulus among an array of several objects. The BSAT is a valuable addition to existing measures of EFs and can be applied reliably in various groups of clinical patients (van Den Berg et al., 2009). The HBTs are quick and easy to administer and can be performed at the bedside compared with other classical measures of EF, such as the Wisconsin Card Sorting test (WCST; Heaton, 1981), Tower of London (ToL; Shallice, 1982), Trail Making test, Part B (TMT-B; Reitan, 1958), and Behavioural Assessment of the Dysexecutive Syndrome (BADS; Wilson, Alderman, Burgess, Emslie, & Evans, 1996)—all of which are longer and more difficult. Several issues can be raised concerning the shortness of this battery; nevertheless, its positive features have rendered it an exceptional instrument in clinical protocols (Bagshaw, Gray, & Snowden, 2014; Rose, Davis, Frampton, & Lask, 2011; Shallice et al., 2002; Spitzer, White, Mandy, & Burgess, 2017; Wood & Liossi, 2006; 2007) and experimental studies (Cipolotti et al., 2016; Harvey, Rose, Jonsson, & Lask, 2016; Macfarlane et al., 2015; Volle et al., 2011). The HBTs have been described to be reliable and psychometrically valid (Bayard et al., 2017; Bielak, Mansueti, Strauss, & Dixon, 2006; Pérez-Pérez et al., 2016; Siqueira, Gonçalves, Hübner, & Fonseca, 2016; Stenbäck, Hällgren, Lyxell, & Larsby, 2015). In this study, we aimed to provide normative data on Italians and adjusted scores for demographic factors (i.e., gender, age, and education) that influence cognitive functions. Methods Description of Hayling and Brixton Tests Hayling Sentence Completion test The HSCT consists of 30 sentences and is divided into two sections (1 and 2) with 15 sentences each, all of which are missing the last word. The sentences provide a semantically forced perspective, such that participants quickly and automatically produce a specific word that completes the sentence (i.e., When you go to bed, turn off the…? –light–). In the first condition (automatic condition), participants are asked to complete the sentences properly, thus reflecting the initiation of a semantically supported automatic response. In the second condition (inhibition condition), participants complete the sentence with an entirely unrelated item, desisting from using the spontaneously triggered word. The participants’ response latencies for both sections were recorded using a stopwatch. Outcome measures included response latencies for Sections 1 and 2 and two categories of connected response error scores (error A and error B) in Section 2. Responses in Section 2 were scored accordingly to Burgess and Shallice (1997): category A errors were responses that reasonably completed the sentence (i.e., The dough was put in the hot…–pot–); category B errors were those that were linked tangentially to the sentence but not a direct or obvious completion (i.e., Most sharks attack very close to…. –fish–). The difference, or ratio, between Sections 1 and 2 was an indicator of the ability to inhibit an automatic answer. In accordance with Burgess and Shallice (1997), the latency for each sentence was rounded down to the nearest second (i.e., response times from 0.00 to 0.99 s were rounded down to 0 s), and the latency time for the overlearned task in Section 1 was generally 0 s. Thus, to analyze the ratio of times between Sections 2 and 1 (according to Pérez-Pérez et al., 2016), we added a constant and obtained the ratio (S2 + 1)/(S1 + 1) to score the times. Similarly, the final error score in Section 1 should be 0 for nearly all participants. Thus, to study the ratio in errors between Sections 2 (E2) and 1 (E1), we added 1 point to both values to establish norms for scoring errors: (E2 + 1)/(E1 + 1). E2 is the sum of Category A errors (connected) and Category B errors (somewhat connected). Brixton Spatial Anticipation test In the BSAT, the participant is required to detect a “visuo-spatial rule” in a sequence of 56 stimulus pages. Each stimulus contains an array of 10 circles (two rows of five circles). On each page, one circle is filled in blue. The position of the blue circle shifts between pages, and the participant must decipher the rule that governs the sequence of changes and predicting the location of the filled circle in the next trial. As the test proceeds, the rule changes, requiring him to deduce the new rule. Responses are considered to be correct if they followed the current rule, and in trials in which the rule changed, a response was correct if it followed the previous rule. The rule changed between stimuli, and the subject had to guess the new rule. Because the BSAT yields a raw accuracy score, we considered the number of errors to be the outcome measure. Development of the Test Pilot study: tuning the sentences from English to Italian To use the HSCT, a pilot study was conducted to ensure that most participants translated the sentences into Italian similarly and, in particular, that the sentences were completed using similar words. In the pilot study, 60 participants (33 women; mean age 37.24 ± 11.05) were asked to provide the final word for 54 incomplete sentences, 34 of which were translated from the original British protocol; the remaining 20 were developed by researchers. Thirty-four sentences were selected from this set, based on each having been completed by all of the participants using the identical word in the pilot study. Four sentences were replaced by four Italian sentences, because they were untranslatable idiomatic sentences. Items were then assigned to the automatic or inhibition condition following the original British subdivision. Design To ensure that the criteria for the administration of the tests, the data recording and the scoring procedures were uniform, six examiners participated in a collective training program of eight sessions, each lasting 2 hr. The same examiner assessed the participants at each site. Participants underwent approximately 45 min of testing over one session, and the order of the tests was balanced between participants. The HBTs were administered as part of a larger neuropsychological battery, including the Mini Mental State Examination (MMSE, Folstein, Folstein, & McHugh., 1975), Raven’s Colored Progressive Matrices (Raven, 1938), and Verbal Judgments (Spinnler & Tognoni, 1987). These latter three tests were administered to exclude participants with cognitive declines or deficits in verbal and visuo-spatial reasoning. Participants A total of 301 participants were enrolled from March 2014 to September 2016. Subjects were recruited by word of mouth and flyers that were distributed throughout the university area (i.e., bookshops, cafeterias, and public library) and community meeting points (primarily the library, sports clubs, activity centers for elderly people, and churches). After contacting the experimenter, participants received an information sheet that explained the procedures and goals of the study and the exclusion criteria. When they became eligible and were still willing to participate, they were invited to visit the university laboratory. The inclusion criteria were: age between 16 and 99 years, absence of any cognitive or functional impairment, Italian as the native language; and normal or corrected non-normal vision and hearing. The exclusion criteria were: any neurological or major psychiatric illness, the use of psychotropic medications, previous traumatic brain injury, history of learning disabilities, alcohol or drug abuse, subjective complaints of cognitive impairment, Mini Mental State Examination score <26, and any major medical illness. Of the initial sample, 61 participants were excluded, because they did not meet the inclusion criteria (see Table 1). Table 1. Exclusion criteria and number of participants excluded per the specified exclusion criteria Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Note: OSAS = Obstruction Sleep Apnea Syndrome; equivalent score (E.S.): 4-1 = within normal range; 0 = under the normal range (Spinnler & Tognoni, 1987) Table 1. Exclusion criteria and number of participants excluded per the specified exclusion criteria Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Note: OSAS = Obstruction Sleep Apnea Syndrome; equivalent score (E.S.): 4-1 = within normal range; 0 = under the normal range (Spinnler & Tognoni, 1987) The final sample comprised 240 healthy participants (109 males and 131 females) aged between 16 and 90 years (mean = 45.80 years, SD = 18.83 years) who were recruited from the communities of four Italian urban towns (Rome, L’Aquila, Monza, and Florence). Among them, 14% had lived in one of the four towns but were born and raised in southern areas. All subjects volunteered to participate and gave their informed consent. Their level of full-time education ranged between 3 and 18 years (mean = 12.29 years, SD = 4.05 years). Regarding the demographics (i.e., gender, education, and sociocultural level), the sample aligned well with Italian census results (15th Population and Housing Census, 2011). The study was approved by the ethical committee of the Department of Psychology, Sapienza, University of Rome. Data Analysis and Statistical Strategy Statistical analyses were performed using IBM SPSS Statistics 20.0. All data were examined for normality (skewness and kurtosis) and restriction of range for age in relation to the dependent variables. Inter-rater Reliability of the HSCT Because the original protocol of the HSCT had been modified, replacing four of the original sentences with four Italian phrases, the reliability of the protocol had to be determined. To this end, 63 participants from the original sample were selected to measure the inter-rater reliability. Three pairs (two raters for each pair) of trained examiners were enrolled for this analysis. Each pair made a conjoint administration of the HBT with the same subject and independently registered his performance and scored the protocol. The administration was balanced between each pair of examiners. Effect of Demographics In the first step, multivariate analysis of variance (MANOVA) was performed to study the effects of gender, age, and education on variables in the HBTs. To interpret the effect size, we used eta squared values (η2) (η2 > 0.01 = small effect; η2 > 0.06 = medium effect; and η2 > 0.14 = large effect) (Richardson, 2011). To obtain the broadest normative data and maximize the clinical application of this study, we used overlapping midpoint age ranges to for the various groups, as suggested by Pauker (1988) and used successfully in several normative studies (Bielak et al., 2006; Pérez-Pérez et al., 2016). In our study, six 20-year age intervals were created to establish norms for an age range of 10 years at the midpoint, except for two extreme ranges in the sample: 16–30 with a midpoint of 22.5 for a normative range of 16–29; 25–44 with a midpoint of 34.5 for a normative range of 30–39; 35–54 with a midpoint of 44.5 for a normative range of 40–49; 45–64 with a midpoint of 54.5 for a normative range of 50–59; 55–74 with a midpoint of 64.5 for a normative range of 60–69; and 65–90 with a midpoint of 74.5 for a normative range of 70–90. Table 2 shows the demographics of the final sample. Table 2. Demographic variables of the final sample and age midpoints Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Note: Education = sum of completed years of school. Table 2. Demographic variables of the final sample and age midpoints Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Note: Education = sum of completed years of school. In the second step, we studied effects of age, gender, and education on Hayling and Brixton variables to provide the Italian norms for the six age ranges, in particular for the four Hayling test variables (times to Sections 1 and 2, Category A and B errors) and for the one Brixton test variable (error scores). As seen in Table 3, we have provided means, standard deviations, and percentiles for each age range and dependent variable. Table 3. Hayling and Brixton tests: means, standard deviations, and percentiles for response latencies and error scores by age range Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Table 3. Hayling and Brixton tests: means, standard deviations, and percentiles for response latencies and error scores by age range Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 In the third step, we determined the age-adjusted norms (means and standard deviations) of the following indicators for the HSCT: time score (S2 + 1)/(S1 + 1) and error score (E2 + 1)/(E1 + 1). To this end, the raw time and error scores were first converted into percentile ranks for each age distribution and then transformed into scaled scores (from 1 to 19, mean 10 and SD 3). Next, linear regression analysis was performed to examine the type of relationship between age and the two variables. Continuous norming (Gorsuch, 1983) was used to estimate the scaled scores, adjusted by age. Results Inter-rater Reliability The internal consistency (Cronbach’s α) of each of pair of raters ranged between 0.83 and 0.85. Cohen’s kappa (κ statistics) of the inter-rater reliability was 0.95 for the error score A and 0.83 for error score B. For the response times, the κ values were 0.77 for time in Section 1 and 0.82 for time in Section 2. According to Nunnally and Bernstein (1994), these indices are good to excellent. Effect of Demographics Table 3 shows the mean and standard deviation for all HBT variables. By MANOVA, age had a strong effect on both tests and education had a small effect only on reaction time for Section 1, with age (6 levels), education (3 levels: 5–8 years, 9–13 years, and 14–18 years), and gender (2 levels) as categorical variables and performance on the HBTs as a continuous dependent variable. There were no interactions or gender effects [age × gender: F(20, 667.59) = 1.135, p = .309, η2 = .03; age × education: F(45, 902.22) = 1.196, p = 180, η2 = .05; gender × education: F(5, 201) = 0.693, p = 630, η2 = .01; age × gender × education: F(45, 902.22) = 0.819, p = 797, η2 = .03; gender: F(5, 234) = 0.603, p = 698, η2 = .01]. We found that age significantly affected the following variables on the HSCTs: – Time in Section 1, F(5, 234) = 36.90, p < .001, η2 = .44 – Time in Section 2, F(5, 234) = 7.22, p < .001, η2 = .13 – Category A errors in Section 2, F(5, 234) = 7.35, p < .001, η2 = .14 For the Brixton test, we noted a significant effect of age on the number of errors [F(5, 234) = 4.37, p < .001, η2 = .08]. Education had only a small effect on time in Section 1 (F(2, 237) = 4.48, p < .05, η2 = .03) of the HSCT. Italian norms We provided Italian norms for six age ranges, specifically for the four Hayling test variables (times in Sections 1 and 2, Category A and B errors) and the one Brixton test variable (error score). Table 3 shows the means, standard deviations, and percentiles for these factors. Tables 4 and 5 show the age-adjusted time scores (S2 + 1)/(S1 + 1) and error scores (E2 + 1)/(E1 + 1) on the HSCT, respectively. Table 4. Age-adjusted scores for Hayling (S2 + 1)/(S1 + 1) time scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 4. Age-adjusted scores for Hayling (S2 + 1)/(S1 + 1) time scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 5. Age-adjusted scores for Hayling (E2 + 1)/(E1 + 1) error scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 5. Age-adjusted scores for Hayling (E2 + 1)/(E1 + 1) error scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Discussion The HBTs, created by Burgess and Shallice (1996, 1997), constitute a brief neuropsychological battery for the assessment of verbal and spatial inhibition and flexibility. This battery is composed of two tests: the HSCT and BSAT. Both tests have shown high construct validity and strong reliability in clinical and experimental settings. The HSCT is a measure of response initiation and response suppression, based entirely on verbal modality. Thus, the HSCT has been adapted for several languages (Bayard et al., 2017; Bielak et al., 2006; Pérez-Pérez et al., 2016; Siqueira et al., 2016). In this study, we translated most of the sentences and changed four idiomatic expressions to conform the HSCT to Italian. Consequently, the Italian protocol demonstrated that the new set of sentences on the HSCT maintained strong reliability, based on Cronbach’s alpha. Further, we have generated psychometric and normative data for the HBTs in a sample of 240 healthy Italian-speaking participants from four Italian regions. Finally, we have provided readers with normative data for HBT variables and the norms of age-adjusted scores for two additional indices of the HSCT: time score and error score. These latter proportional variables are particularly important in the clinical assessment of executive functioning (Andrés & Van der Linden, 2000). Normative Data and Effect of Demographics We estimated the effects of age, education, and gender on performance on the HBTs. Age had an effect on three variables of the HSCT: time in Section 1, time in Section 2, and A-type errors in Section 2. The data also showed that as age increased, the response times slowed, and category A errors and the number of errors on the BSAT rose. Regarding the two additional variables of the HSCT [time score (S2 + 1)/(S1 + 1) and error score(E2 + 1)/(E1 + 1)], as age increased, time scores (S2 + 1)/(S1 + 1) declined while error scores (E2 + 1)/(E1 + 1) climbed. These results are consistent with previous research on the effects of age on speed processing and verbal inhibition (Andrés & Van der Linden, 2000; Pérez-Pérez et al., 2016). Moreover, they support the importance of the prefrontal network in healthy elderly individuals. Proxies of cognitive reserve are associated with a wide network of areas, including the medial and lateral frontal areas—i.e., the anterior cingulate cortex and dorsolateral prefrontal cortex—and the precuneus (Colangeli et al., 2016), the same areas that are involved in performance on the HSCT (Cipolotti et al., 2016; Collette et al., 2001). Neuropsychological tests on inhibition activate the prefrontal network, and deficits in inhibition might affect the performance on other EF components, such as planning (e.g., Goel & Grafman, 1995; Welsh, Satterlee-Cartmell, & Stine, 1999). Regarding the influence of education level, high school education was associated with faster responses in time on Section 1 of the HSCT. Finally, no associations were found between performance on the HBTs and gender, consistent with other studies (Bielak et al., 2006). Applicability and Value of the HBTs The value of this brief battery has been demonstrated throughout this study. Nevertheless, several features of the HBTs are notable. Both tests can be administered quickly, allowing clinicians to use them whenever they need to assess EFs in a short time (i.e., patients who suffer from weariness). Also, the HBTs can be considered a “bedside” battery that facilitates the assessment of patients who are bedridden (e.g., early cognitive assessment), which is particularly important in a clinical evaluation. The HSCT is appropriate for patients with a wide range of problems, such as those that involve reading, visual perception, or motor deficits. Also, one must consider that altered performance on the HSCT has been described in several neurological, psychiatric, and neurodevelopmental conditions, such as Alzheimer disease and mild cognitive impairments (Bayard, Jacus, Raffard, & Gely-Nargeot, 2014; Belleville, Rouleau, & Van der Linden, 2006), traumatic brain injury (Dymowski et al., 2015), cerebrovascular accidents (Robinson et al., 2015), Parkinson disease (Obeso et al., 2011), schizophrenia, bipolar disorder (Martin, Mowry, Reutens, & Robinson, 2015), and autism spectrum disorder (Zimmerman, Ownsworth, O’Donovan, Roberts, & Gullo, 2016). The HSCT has been adopted to measure attentional bias and cognitive disinhibition in alcoholism (Rose, Mason-Li, Nicholas, & Hobbs, 2010). The Brixton test has been used recently in studies on confabulation in autism (Spitzer et al., 2017), training for early-stage Alzheimer disease (Cavallo, Hunter, van der Hiele, & Angilletta et al., 2016), and anorexia nervosa (Abbate-Daga et al., 2015). One must consider that patients with frontal lesions might perform poorly on general EF tests due to their difficulties in inhibiting a strong automatic response (Roberts & Pennington, 1996)—thus, this brief battery might help clinicians in making differential diagnoses. Limitations Our study has several limitations. Our sample included participants from only four Italian regions, primarily from the northern-central Italy, which might have influenced their word choice and limiting the heterogeneity and, thus, representativeness of the sample. Ideally, a random sampling method across the country would have been preferable, maximizing the representativeness of the sample. However, because 14% of participants were born and raised in southern regions, we believe that the risk of using dialectical words was indirectly controlled. Nevertheless, when clinicians adopt the HSCT, they should be aware of this limitation. Another limitation was the small number of participants in each age-education cluster. Thus, to maximize the amount of useful information, we used overlapping cell tables (Pauker, 1988); this technique is particularly appropriate when the sample sizes are small. We also used continuous norming to estimate the scaled scores, adjusted by age; this procedure was introduced as an alternative to the inherent inaccuracies of traditional norming and is better suited for tabled norms—this method was developed by Gorsuch (1983) to mitigate the effects of small sample sizes across age groups. Although our sample was not large, it was similar to the cohorts in other normative studies (Burgess & Shallice, 1997: 121 healthy individuals aged between 18 and 80 years; Pérez-Pérez et al., 2016: 185 healthy individuals aged between 18 and 99 years). Another limitation was the absence of data on the socioeconomic status and occupation of the participants. Finally, a comparison with brain-damaged patients or another clinical population might be provided additional information about the types of errors. Conclusions The main objective of this study was to propose a norm-based adaptation of the HBTs in Italian, becoming the first report to establish normative data for full testing in the Italian population. Our results encourage the use of normative data in neuropsychological assessments and, in particular, in the evaluation of verbal inhibition with the HSCT (Bielak et al., 2006; Tournier, Postal, & Mathey, 2014). 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Normative Data for the Hayling and Brixton Tests in an Italian Population

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Abstract

Abstract Objective The Hayling and Brixton tests constitute a short test battery that quickly assesses verbal and spatial inhibition and flexibility. This battery has shown high construct validity and strong reliability in clinical and experimental settings. The aim of this study was to develop an Italian version of the Hayling and Brixton tests and obtain normative values. Method We collected normative data from 301 healthy Italian participants aged between 16 and 94 years, taking into account all demographics. To maximize the sample size, we used the overlapping interval strategy. Adjusted scores for demographics were obtained by linear regression analysis. Results The performance on the Hayling and Brixton tests was influenced by age and education. In particular, age affected verbal accuracy and response time on the Hayling Sentence Completion Test, whereas education only affected the former. Differently, the spatial component, as measured by the Brixton Spatial Anticipation Test, was shaped only by age, which decreased the number of correct responses. Conclusions Our study provides normative data that have been adjusted for relevant demographics and percentile grids in an Italian population. Our data support the use of the Hayling and Brixton tests as a valid instrument for performing neuropsychological evaluations and longitudinal analyses of executive functions in clinical practice and for research purposes. Executive functions, Hayling test, Brixton test, Neuropsychological assessment, Verbal suppression, Normative data Introduction Executive functions (EFs) refer to higher-order cognitive abilities that regulate and monitor most of our everyday actions, and they are considered to implicate a frontal–parietal network (Niendam et al., 2012) that is engaged throughout various cognitive tasks (Fedorenko, Duncan, & Kanwisher, 2013). Deficiencies in EFs occur frequently after brain damage (Azouvi et al., 2016; Bosco, Parola, Sacco, Zettin, & Angeleri, 2017; Cerezo García, Martín Plasencia, & Aladro Benito, 2015; Chung, Pollock, Campbell, Durward, & Hagen, 2013; Jelcic et al., 2013; Kennedy et al., 2008; Roman & Arnett, 2016), in psychiatric disorders (Bédard, Joyal, Godbout, & Chantal, 2009; David, Soeiro-de-Souza, Moreno, & Bio, 2014; Sharp, Miller, & Heller, 2015; Simon, Berger, Giacomini, Ferrero, & Mohr, 2006; van Beilen, van Zomeren, van den Bosch, Withaar, & Bouma, 2005; Vandborg, Hartmann, Bennedsen, Pedersen, & Thomsen, 2014; Zebdi, Goyet, Pinabiaux, & Guellaï, 2016), and in relation to aging (Mac Kay, 2016; Potter, McQuoid, Whitson, & Steffens, 2015; Turner & Spreng, 2012). Thus, for over six decades, the assessment of EFs has continued to be a significant issue. Impairments in EFs can cause deficits in response initiation and response suppression and on the rule detection task. Burgess and Shallice (1996, 1997) focused on these fundamental executive processes when they developed the Hayling and Brixton tests (HBTs). In the Hayling Sentence Completion test (HSCT), participants are asked to complete several sentences as fast as possible and required to produce or inhibit an automatic response. The response inhibition that is evoked by the HSCT is associated with increased activation of a network of left prefrontal areas (Cipolotti et al., 2016; Collette et al., 2001), and patients with executive dysfunctions perform poorly on this test (Corben et al., 2017; Dymowski, Owens, Ponsford, & Willmott, 2015; Robinson et al., 2015). The Brixton Spatial Anticipation test (BSAT; Burgess & Shallice, 1996) is a rule detection task in which participants must forecast the position of a colored stimulus among an array of several objects. The BSAT is a valuable addition to existing measures of EFs and can be applied reliably in various groups of clinical patients (van Den Berg et al., 2009). The HBTs are quick and easy to administer and can be performed at the bedside compared with other classical measures of EF, such as the Wisconsin Card Sorting test (WCST; Heaton, 1981), Tower of London (ToL; Shallice, 1982), Trail Making test, Part B (TMT-B; Reitan, 1958), and Behavioural Assessment of the Dysexecutive Syndrome (BADS; Wilson, Alderman, Burgess, Emslie, & Evans, 1996)—all of which are longer and more difficult. Several issues can be raised concerning the shortness of this battery; nevertheless, its positive features have rendered it an exceptional instrument in clinical protocols (Bagshaw, Gray, & Snowden, 2014; Rose, Davis, Frampton, & Lask, 2011; Shallice et al., 2002; Spitzer, White, Mandy, & Burgess, 2017; Wood & Liossi, 2006; 2007) and experimental studies (Cipolotti et al., 2016; Harvey, Rose, Jonsson, & Lask, 2016; Macfarlane et al., 2015; Volle et al., 2011). The HBTs have been described to be reliable and psychometrically valid (Bayard et al., 2017; Bielak, Mansueti, Strauss, & Dixon, 2006; Pérez-Pérez et al., 2016; Siqueira, Gonçalves, Hübner, & Fonseca, 2016; Stenbäck, Hällgren, Lyxell, & Larsby, 2015). In this study, we aimed to provide normative data on Italians and adjusted scores for demographic factors (i.e., gender, age, and education) that influence cognitive functions. Methods Description of Hayling and Brixton Tests Hayling Sentence Completion test The HSCT consists of 30 sentences and is divided into two sections (1 and 2) with 15 sentences each, all of which are missing the last word. The sentences provide a semantically forced perspective, such that participants quickly and automatically produce a specific word that completes the sentence (i.e., When you go to bed, turn off the…? –light–). In the first condition (automatic condition), participants are asked to complete the sentences properly, thus reflecting the initiation of a semantically supported automatic response. In the second condition (inhibition condition), participants complete the sentence with an entirely unrelated item, desisting from using the spontaneously triggered word. The participants’ response latencies for both sections were recorded using a stopwatch. Outcome measures included response latencies for Sections 1 and 2 and two categories of connected response error scores (error A and error B) in Section 2. Responses in Section 2 were scored accordingly to Burgess and Shallice (1997): category A errors were responses that reasonably completed the sentence (i.e., The dough was put in the hot…–pot–); category B errors were those that were linked tangentially to the sentence but not a direct or obvious completion (i.e., Most sharks attack very close to…. –fish–). The difference, or ratio, between Sections 1 and 2 was an indicator of the ability to inhibit an automatic answer. In accordance with Burgess and Shallice (1997), the latency for each sentence was rounded down to the nearest second (i.e., response times from 0.00 to 0.99 s were rounded down to 0 s), and the latency time for the overlearned task in Section 1 was generally 0 s. Thus, to analyze the ratio of times between Sections 2 and 1 (according to Pérez-Pérez et al., 2016), we added a constant and obtained the ratio (S2 + 1)/(S1 + 1) to score the times. Similarly, the final error score in Section 1 should be 0 for nearly all participants. Thus, to study the ratio in errors between Sections 2 (E2) and 1 (E1), we added 1 point to both values to establish norms for scoring errors: (E2 + 1)/(E1 + 1). E2 is the sum of Category A errors (connected) and Category B errors (somewhat connected). Brixton Spatial Anticipation test In the BSAT, the participant is required to detect a “visuo-spatial rule” in a sequence of 56 stimulus pages. Each stimulus contains an array of 10 circles (two rows of five circles). On each page, one circle is filled in blue. The position of the blue circle shifts between pages, and the participant must decipher the rule that governs the sequence of changes and predicting the location of the filled circle in the next trial. As the test proceeds, the rule changes, requiring him to deduce the new rule. Responses are considered to be correct if they followed the current rule, and in trials in which the rule changed, a response was correct if it followed the previous rule. The rule changed between stimuli, and the subject had to guess the new rule. Because the BSAT yields a raw accuracy score, we considered the number of errors to be the outcome measure. Development of the Test Pilot study: tuning the sentences from English to Italian To use the HSCT, a pilot study was conducted to ensure that most participants translated the sentences into Italian similarly and, in particular, that the sentences were completed using similar words. In the pilot study, 60 participants (33 women; mean age 37.24 ± 11.05) were asked to provide the final word for 54 incomplete sentences, 34 of which were translated from the original British protocol; the remaining 20 were developed by researchers. Thirty-four sentences were selected from this set, based on each having been completed by all of the participants using the identical word in the pilot study. Four sentences were replaced by four Italian sentences, because they were untranslatable idiomatic sentences. Items were then assigned to the automatic or inhibition condition following the original British subdivision. Design To ensure that the criteria for the administration of the tests, the data recording and the scoring procedures were uniform, six examiners participated in a collective training program of eight sessions, each lasting 2 hr. The same examiner assessed the participants at each site. Participants underwent approximately 45 min of testing over one session, and the order of the tests was balanced between participants. The HBTs were administered as part of a larger neuropsychological battery, including the Mini Mental State Examination (MMSE, Folstein, Folstein, & McHugh., 1975), Raven’s Colored Progressive Matrices (Raven, 1938), and Verbal Judgments (Spinnler & Tognoni, 1987). These latter three tests were administered to exclude participants with cognitive declines or deficits in verbal and visuo-spatial reasoning. Participants A total of 301 participants were enrolled from March 2014 to September 2016. Subjects were recruited by word of mouth and flyers that were distributed throughout the university area (i.e., bookshops, cafeterias, and public library) and community meeting points (primarily the library, sports clubs, activity centers for elderly people, and churches). After contacting the experimenter, participants received an information sheet that explained the procedures and goals of the study and the exclusion criteria. When they became eligible and were still willing to participate, they were invited to visit the university laboratory. The inclusion criteria were: age between 16 and 99 years, absence of any cognitive or functional impairment, Italian as the native language; and normal or corrected non-normal vision and hearing. The exclusion criteria were: any neurological or major psychiatric illness, the use of psychotropic medications, previous traumatic brain injury, history of learning disabilities, alcohol or drug abuse, subjective complaints of cognitive impairment, Mini Mental State Examination score <26, and any major medical illness. Of the initial sample, 61 participants were excluded, because they did not meet the inclusion criteria (see Table 1). Table 1. Exclusion criteria and number of participants excluded per the specified exclusion criteria Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Note: OSAS = Obstruction Sleep Apnea Syndrome; equivalent score (E.S.): 4-1 = within normal range; 0 = under the normal range (Spinnler & Tognoni, 1987) Table 1. Exclusion criteria and number of participants excluded per the specified exclusion criteria Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Exclusion criteria N Details Mini Mental State Examination score <26 5 Cognitive decline Raven <4 (equivalent score) 1 E.S. = 0 Verbal judgments <4 (equivalent score) 1 E.S. = 0 Neurological disease 8 – Vascular disease = 5 – Multiple sclerosis = 1 – Previous meningioma = 1 – Parkinson disease = 1 Major psychiatric illness or use of psychopharmacological therapy depression, anxiety disorder 12 – Major depression = 5 – Anxiety disorder = 6 – Bipolar disorder = 1 Subjective complaint of cognitive impairment 10 – Cognitive fatigue = 3 – Memory loss = 2 – Deficits in sustained attention = 5 Major medical illness 16 – Stutter = 2 – Obesity and OSAS = 5 – Hypertension = 9 Drug abuse in the past 1 Alcohol abuse Impaired hearing 2 Not corrected Italian not native language 5 – English = 1 – Spanish = 1 – Romanian = 3 Note: OSAS = Obstruction Sleep Apnea Syndrome; equivalent score (E.S.): 4-1 = within normal range; 0 = under the normal range (Spinnler & Tognoni, 1987) The final sample comprised 240 healthy participants (109 males and 131 females) aged between 16 and 90 years (mean = 45.80 years, SD = 18.83 years) who were recruited from the communities of four Italian urban towns (Rome, L’Aquila, Monza, and Florence). Among them, 14% had lived in one of the four towns but were born and raised in southern areas. All subjects volunteered to participate and gave their informed consent. Their level of full-time education ranged between 3 and 18 years (mean = 12.29 years, SD = 4.05 years). Regarding the demographics (i.e., gender, education, and sociocultural level), the sample aligned well with Italian census results (15th Population and Housing Census, 2011). The study was approved by the ethical committee of the Department of Psychology, Sapienza, University of Rome. Data Analysis and Statistical Strategy Statistical analyses were performed using IBM SPSS Statistics 20.0. All data were examined for normality (skewness and kurtosis) and restriction of range for age in relation to the dependent variables. Inter-rater Reliability of the HSCT Because the original protocol of the HSCT had been modified, replacing four of the original sentences with four Italian phrases, the reliability of the protocol had to be determined. To this end, 63 participants from the original sample were selected to measure the inter-rater reliability. Three pairs (two raters for each pair) of trained examiners were enrolled for this analysis. Each pair made a conjoint administration of the HBT with the same subject and independently registered his performance and scored the protocol. The administration was balanced between each pair of examiners. Effect of Demographics In the first step, multivariate analysis of variance (MANOVA) was performed to study the effects of gender, age, and education on variables in the HBTs. To interpret the effect size, we used eta squared values (η2) (η2 > 0.01 = small effect; η2 > 0.06 = medium effect; and η2 > 0.14 = large effect) (Richardson, 2011). To obtain the broadest normative data and maximize the clinical application of this study, we used overlapping midpoint age ranges to for the various groups, as suggested by Pauker (1988) and used successfully in several normative studies (Bielak et al., 2006; Pérez-Pérez et al., 2016). In our study, six 20-year age intervals were created to establish norms for an age range of 10 years at the midpoint, except for two extreme ranges in the sample: 16–30 with a midpoint of 22.5 for a normative range of 16–29; 25–44 with a midpoint of 34.5 for a normative range of 30–39; 35–54 with a midpoint of 44.5 for a normative range of 40–49; 45–64 with a midpoint of 54.5 for a normative range of 50–59; 55–74 with a midpoint of 64.5 for a normative range of 60–69; and 65–90 with a midpoint of 74.5 for a normative range of 70–90. Table 2 shows the demographics of the final sample. Table 2. Demographic variables of the final sample and age midpoints Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Note: Education = sum of completed years of school. Table 2. Demographic variables of the final sample and age midpoints Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) N 50 62 70 75 65 41 Age  M 22.70 32.52 45.23 54.28 62.49 72.85  SD 4.79 5.26 6.33 5.42 5.56 6.84 Gender  Women 28 30 39 43 34 22  Men 22 32 31 32 31 19 Education  M 13.24 14.91 12.79 11.39 11.21 9.73  SD 3.07 3.06 3.27 3.40 4.50 5.00 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Note: Education = sum of completed years of school. In the second step, we studied effects of age, gender, and education on Hayling and Brixton variables to provide the Italian norms for the six age ranges, in particular for the four Hayling test variables (times to Sections 1 and 2, Category A and B errors) and for the one Brixton test variable (error scores). As seen in Table 3, we have provided means, standard deviations, and percentiles for each age range and dependent variable. Table 3. Hayling and Brixton tests: means, standard deviations, and percentiles for response latencies and error scores by age range Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Table 3. Hayling and Brixton tests: means, standard deviations, and percentiles for response latencies and error scores by age range Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Variable Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Hayling test Time to Section 1 (S1) M ± SD 2.80 ± 2.78 2.21 ± 2.21 6.56 ± 6.81 9.04 ± 6.82 11.26 ± 6.54 14.83 ± 5.80 Percentiles  5° 7 6 20 18 19 24  25° 5 4 15 15 16 17  50° 2 2 4 8 15 15  75° 0 0 0 3 5 12  95° 0 0 0 0 0 5 Time to Section 2 (S2) M ± SD 15.22 ± 14.37 16.35 ± 13.46 22.73 ± 17.60 26.91 ± 14.74 34.86 ± 20.20 47.56 ± 29.07 Percentiles  5° 44 46 62 60 80 109  25° 25 26 30 36 45 58  50° 10 12 21 24 31 39  75° 3 5 9 16 21 27  95° 0 0 1 6 11 14 Category A errors M ± SD 0.90 ± 1.42 0.73 ± 1.16 1.59 ± 2.07 2.23 ± 2.65 2.83 ± 3.09 4.29 ± 4.18 Percentiles  5° 4 3 6 7 9 11  25° 2 1 3 4 5 7  50° 0 0 1 1 1 3  75° 0 0 0 0 0 1  95° 0 0 0 0 0 0 Category B errors M ± SD 3.00 ± 2.56 3.69 ± 2.92 4.56 ± 3.39 4.23 ± 3.21 4.35 ± 3.20 4.20 ± 2.68 Percentiles  5° 8 9 10 9 9 9  25° 5 5 7 7 7 6  50° 3 3 4 4 4 4  75° 1 1 2 2 2 3  95° 0 0 0 0 0 0 Brixton test Error score M ± SD 15.68 ± 4.34 15.32 ± 6.8 16.06 ± 6.42 16.36 ± 6.19 18.11 ± 8.44 21.24 ± 9.14 Percentiles  5° 40 24 29 27 38 37  25° 17 17 19 19 20 23  50° 14 14 15 15 15 19  75° 12 11 11 12 13 14  95° 8 7 8 9 9 11 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 In the third step, we determined the age-adjusted norms (means and standard deviations) of the following indicators for the HSCT: time score (S2 + 1)/(S1 + 1) and error score (E2 + 1)/(E1 + 1). To this end, the raw time and error scores were first converted into percentile ranks for each age distribution and then transformed into scaled scores (from 1 to 19, mean 10 and SD 3). Next, linear regression analysis was performed to examine the type of relationship between age and the two variables. Continuous norming (Gorsuch, 1983) was used to estimate the scaled scores, adjusted by age. Results Inter-rater Reliability The internal consistency (Cronbach’s α) of each of pair of raters ranged between 0.83 and 0.85. Cohen’s kappa (κ statistics) of the inter-rater reliability was 0.95 for the error score A and 0.83 for error score B. For the response times, the κ values were 0.77 for time in Section 1 and 0.82 for time in Section 2. According to Nunnally and Bernstein (1994), these indices are good to excellent. Effect of Demographics Table 3 shows the mean and standard deviation for all HBT variables. By MANOVA, age had a strong effect on both tests and education had a small effect only on reaction time for Section 1, with age (6 levels), education (3 levels: 5–8 years, 9–13 years, and 14–18 years), and gender (2 levels) as categorical variables and performance on the HBTs as a continuous dependent variable. There were no interactions or gender effects [age × gender: F(20, 667.59) = 1.135, p = .309, η2 = .03; age × education: F(45, 902.22) = 1.196, p = 180, η2 = .05; gender × education: F(5, 201) = 0.693, p = 630, η2 = .01; age × gender × education: F(45, 902.22) = 0.819, p = 797, η2 = .03; gender: F(5, 234) = 0.603, p = 698, η2 = .01]. We found that age significantly affected the following variables on the HSCTs: – Time in Section 1, F(5, 234) = 36.90, p < .001, η2 = .44 – Time in Section 2, F(5, 234) = 7.22, p < .001, η2 = .13 – Category A errors in Section 2, F(5, 234) = 7.35, p < .001, η2 = .14 For the Brixton test, we noted a significant effect of age on the number of errors [F(5, 234) = 4.37, p < .001, η2 = .08]. Education had only a small effect on time in Section 1 (F(2, 237) = 4.48, p < .05, η2 = .03) of the HSCT. Italian norms We provided Italian norms for six age ranges, specifically for the four Hayling test variables (times in Sections 1 and 2, Category A and B errors) and the one Brixton test variable (error score). Table 3 shows the means, standard deviations, and percentiles for these factors. Tables 4 and 5 show the age-adjusted time scores (S2 + 1)/(S1 + 1) and error scores (E2 + 1)/(E1 + 1) on the HSCT, respectively. Table 4. Age-adjusted scores for Hayling (S2 + 1)/(S1 + 1) time scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 4. Age-adjusted scores for Hayling (S2 + 1)/(S1 + 1) time scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >23 >20 >18 >16 >14 >10 2 <1 22–23 19–20 17–18 16 14 10 Abnormal 3 1 20–21 18 16 14–15 13 — 4 2 18–19 16–17 14–15 −13 11–12 9 Poor 5 5 16–17 14–15 13 11–12 10 8 Low average 6 9 14–15 12–13 11–12 10 9 7 7 16 12–13 10–11 10 9 8 6 Moderate average 8 25 10–11 9 8–9 7–8 6–7 5 9 37 8–9 7–8 6–7 6 5 4 Average 10 50 6–7 5–6 5 4–5 4 3 11 63 4–5 3–4 3–4 3 3 2 High average 12 75 2–3 2 2 2 2 — 13 84 1 1 1 1 1 1 Good 14 91 — — — — — — Superior 15 95 — — — — — — 16 98 — — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 5. Age-adjusted scores for Hayling (E2 + 1)/(E1 + 1) error scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Table 5. Age-adjusted scores for Hayling (E2 + 1)/(E1 + 1) error scores Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 Classificationa Scaled score Percentile rank Age range 16–29 years (N = 50) 30–39 years (N = 62) 40–49 years (N = 70) 50–59 years (N = 75) 60–69 years (N = 65) 70–90 years (N = 41) Impaired 1 <1 >15 >15 >15 >15 >15 >15 2 <1 14–15 — — — — — Abnormal 3 1 13 15 — — — — 4 2 12 14 15 — — — Poor 5 5 11 12–13 14 15 — — Low average 6 9 10 11 12–13 13–14 15 — 7 16 8–9 10 11 12 13–14 15 Moderate average 8 25 7 8–9 9–10 10–11 11–12 13–14 9 37 6 7 8 9 10 11–12 Average 10 50 5 6 6–7 7–8 8–9 9–10 11 63 4 4–5 5 6 6–7 7–8 High average 12 75 2–3 3 3–4 4–5 4–5 5–6 13 84 1 2 2 2–3 3 3–4 Good 14 91 — 1 1 1 1–2 2 Superior 15 95 — — — — 1 16 98 — — — — — Highly superior 17 99 — — — — — — 18 >99 — — — — — — 19 >99 <1 <1 <1 <1 <1 Age midpoint 22.5 34.5 44.5 54.5 64.5 82.5 aClassification based on scaled score convention used for Hayling and Brixton tests. Discussion The HBTs, created by Burgess and Shallice (1996, 1997), constitute a brief neuropsychological battery for the assessment of verbal and spatial inhibition and flexibility. This battery is composed of two tests: the HSCT and BSAT. Both tests have shown high construct validity and strong reliability in clinical and experimental settings. The HSCT is a measure of response initiation and response suppression, based entirely on verbal modality. Thus, the HSCT has been adapted for several languages (Bayard et al., 2017; Bielak et al., 2006; Pérez-Pérez et al., 2016; Siqueira et al., 2016). In this study, we translated most of the sentences and changed four idiomatic expressions to conform the HSCT to Italian. Consequently, the Italian protocol demonstrated that the new set of sentences on the HSCT maintained strong reliability, based on Cronbach’s alpha. Further, we have generated psychometric and normative data for the HBTs in a sample of 240 healthy Italian-speaking participants from four Italian regions. Finally, we have provided readers with normative data for HBT variables and the norms of age-adjusted scores for two additional indices of the HSCT: time score and error score. These latter proportional variables are particularly important in the clinical assessment of executive functioning (Andrés & Van der Linden, 2000). Normative Data and Effect of Demographics We estimated the effects of age, education, and gender on performance on the HBTs. Age had an effect on three variables of the HSCT: time in Section 1, time in Section 2, and A-type errors in Section 2. The data also showed that as age increased, the response times slowed, and category A errors and the number of errors on the BSAT rose. Regarding the two additional variables of the HSCT [time score (S2 + 1)/(S1 + 1) and error score(E2 + 1)/(E1 + 1)], as age increased, time scores (S2 + 1)/(S1 + 1) declined while error scores (E2 + 1)/(E1 + 1) climbed. These results are consistent with previous research on the effects of age on speed processing and verbal inhibition (Andrés & Van der Linden, 2000; Pérez-Pérez et al., 2016). Moreover, they support the importance of the prefrontal network in healthy elderly individuals. Proxies of cognitive reserve are associated with a wide network of areas, including the medial and lateral frontal areas—i.e., the anterior cingulate cortex and dorsolateral prefrontal cortex—and the precuneus (Colangeli et al., 2016), the same areas that are involved in performance on the HSCT (Cipolotti et al., 2016; Collette et al., 2001). Neuropsychological tests on inhibition activate the prefrontal network, and deficits in inhibition might affect the performance on other EF components, such as planning (e.g., Goel & Grafman, 1995; Welsh, Satterlee-Cartmell, & Stine, 1999). Regarding the influence of education level, high school education was associated with faster responses in time on Section 1 of the HSCT. Finally, no associations were found between performance on the HBTs and gender, consistent with other studies (Bielak et al., 2006). Applicability and Value of the HBTs The value of this brief battery has been demonstrated throughout this study. Nevertheless, several features of the HBTs are notable. Both tests can be administered quickly, allowing clinicians to use them whenever they need to assess EFs in a short time (i.e., patients who suffer from weariness). Also, the HBTs can be considered a “bedside” battery that facilitates the assessment of patients who are bedridden (e.g., early cognitive assessment), which is particularly important in a clinical evaluation. The HSCT is appropriate for patients with a wide range of problems, such as those that involve reading, visual perception, or motor deficits. Also, one must consider that altered performance on the HSCT has been described in several neurological, psychiatric, and neurodevelopmental conditions, such as Alzheimer disease and mild cognitive impairments (Bayard, Jacus, Raffard, & Gely-Nargeot, 2014; Belleville, Rouleau, & Van der Linden, 2006), traumatic brain injury (Dymowski et al., 2015), cerebrovascular accidents (Robinson et al., 2015), Parkinson disease (Obeso et al., 2011), schizophrenia, bipolar disorder (Martin, Mowry, Reutens, & Robinson, 2015), and autism spectrum disorder (Zimmerman, Ownsworth, O’Donovan, Roberts, & Gullo, 2016). The HSCT has been adopted to measure attentional bias and cognitive disinhibition in alcoholism (Rose, Mason-Li, Nicholas, & Hobbs, 2010). The Brixton test has been used recently in studies on confabulation in autism (Spitzer et al., 2017), training for early-stage Alzheimer disease (Cavallo, Hunter, van der Hiele, & Angilletta et al., 2016), and anorexia nervosa (Abbate-Daga et al., 2015). One must consider that patients with frontal lesions might perform poorly on general EF tests due to their difficulties in inhibiting a strong automatic response (Roberts & Pennington, 1996)—thus, this brief battery might help clinicians in making differential diagnoses. Limitations Our study has several limitations. Our sample included participants from only four Italian regions, primarily from the northern-central Italy, which might have influenced their word choice and limiting the heterogeneity and, thus, representativeness of the sample. Ideally, a random sampling method across the country would have been preferable, maximizing the representativeness of the sample. However, because 14% of participants were born and raised in southern regions, we believe that the risk of using dialectical words was indirectly controlled. Nevertheless, when clinicians adopt the HSCT, they should be aware of this limitation. Another limitation was the small number of participants in each age-education cluster. Thus, to maximize the amount of useful information, we used overlapping cell tables (Pauker, 1988); this technique is particularly appropriate when the sample sizes are small. We also used continuous norming to estimate the scaled scores, adjusted by age; this procedure was introduced as an alternative to the inherent inaccuracies of traditional norming and is better suited for tabled norms—this method was developed by Gorsuch (1983) to mitigate the effects of small sample sizes across age groups. Although our sample was not large, it was similar to the cohorts in other normative studies (Burgess & Shallice, 1997: 121 healthy individuals aged between 18 and 80 years; Pérez-Pérez et al., 2016: 185 healthy individuals aged between 18 and 99 years). Another limitation was the absence of data on the socioeconomic status and occupation of the participants. Finally, a comparison with brain-damaged patients or another clinical population might be provided additional information about the types of errors. Conclusions The main objective of this study was to propose a norm-based adaptation of the HBTs in Italian, becoming the first report to establish normative data for full testing in the Italian population. Our results encourage the use of normative data in neuropsychological assessments and, in particular, in the evaluation of verbal inhibition with the HSCT (Bielak et al., 2006; Tournier, Postal, & Mathey, 2014). 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Archives of Clinical NeuropsychologyOxford University Press

Published: Aug 22, 2017

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