Previous studies indicate that autobiographical memory is impaired in individuals with autism spectrum disorder (ASD). Successful recollection of information referring to one’s own person requires the intact ability to re-activate representation of the past self. In the current fMRI study we investigated process of conscious reflection on the present self, the past self, and a close-other in the ASD and typically developing groups. Significant inter-group differences were found in the Past-Self condition. In individuals with ASD, reflection on the past self was associated with additional engagement of the posterior cingulate and posterior temporal structures. We hypothesize that this enhanced activation of widely distributed neural network reflects substantial difficulties in processes of reflection on one’s own person in the past. Keywords fMRI · Self-referential processing · Self-continuity · Autobiographical memory Abbreviationsr Right ACG Anterior cingulate gyrus STG Superior temporal gyrus ASD Autism spectrum disorder group TD Typically developing group fMRI Functional magnetic resonance imagingTPJ Temporoparietal junction IFG Inferior frontal gyrus l Left MCG Middle cingulate gyrus Introduction MFG Middle frontal gyrus MTG Middle temporal gyrus One fundamental feature of the human conscious experi- p Posterior ence is a sense of self that persists across time (Gallagher PCG Posterior cingulate gyrus 2000; Moran et al. 2006; Morin 2006). The sense of self- continuity is related to autobiographical memory and it is based on the ability to consolidate different and temporally * Hanna B. Cygan separated pieces of self-related information into one coher- email@example.com ent whole (McAdams 2001; Conway 2005). However, pro- Laboratory of Social Psychology, Department cessing personal changes across the lifespan requires the of Ergonomics, Central Institute for Labour Protection ability to strictly distinguish between representations of the - National Research Institute, 16 Czerniakowska Street, present and the past selves; this ability was hypothesized to 00-701 Warsaw, Poland be crucial for the formation of a stable identity during the Laboratory of Psychophysiology, Department late adolescence and early adulthood (McAdams 2001). of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, It is noteworthy that several studies on autism spectrum 02-093 Warsaw, Poland disorder (ASD) have reported difficulties in remembering Laboratory of Brain Imaging, Neurobiology Center, the past (Bowler et al. 2007). Specifically, this was the case Nencki Institute of Experimental Biology, Polish Academy for autobiographical memory tasks that assessed the ability of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland to recall personally experienced events and personal seman- Faculty of Humanities, Nicolaus Copernicus University, tic facts (for review see: Brezis 2015). In children with ASD, Torun, Poland both semantic and episodic autobiographical memory is Department of Psychological and Brain Sciences, Dartmouth reduced (Bruck et al. 2007; Bon et al. 2012; Goddard et al. College, Hanover, NH, USA Vol.:(0123456789) 1 3 Journal of Autism and Developmental Disorders 2014). By adulthood, individuals with ASD show a spared Methods memory for semantic autobiographical memory, alongside reduced episodic autobiographical memory (Klein et al. Subjects 1999; Crane and Goddard 2008). Individuals with ASD con- sistently recollect not only fewer events from their past than Fifteen young males with ASD and 15 control subjects matched control subjects but also take substantially longer participated in this study. The clinical diagnosis of indi- to do so (e.g. Goddard et al. 2007; Crane and Goddard 2008; viduals with ASD was confirmed using the Polish trans - Crane et al. 2009; Lind and Bowler 2009; Adler et al. 2010). lation of the Autism Diagnostic Observation Schedule— It was proposed that autobiographical memory difficulties ADOS (module 4) (Lord et al. 2008). The ASD group in this clinical group may be related to a reduction of cogni- was recruited by the psychologists and therapists from the tive resources for auto-noetic awareness, i.e. the conscious SYNAPSIS foundation which provides diagnosis assis- re-experiencing of past events (Tanweer et al. 2010; Crane tance and therapy for people with ASD and their families. et al. 2012). Such disturbed ability to recall the past can Control subjects were matched one-to-one to individu- result in impaired anticipation of and planning for the future, als with ASD in terms of age, sex, handedness, and IQ- which in turn may lead to the lack of flexibility and enhanced score. Subjects’ IQs were evaluated using Polish version anxiety, that is typical for individuals with ASD (Kreslins of the Wechsler Intelligence Scale for Adults—Revised et al. 2015). However, impaired autobiographical memory (WAIS-R, PL) (Brzeziński et al. 2004). The maximal IQ may also be viewed in the light of disturbed self-referential difference between each individual with ASD and the cognition in ASD (e.g. Crane et al. 2009; Lombardo and matched control subject was ± 15 (see Table 1). The maxi- Baron-Cohen 2010; Glezerman 2013; Cygan et al. 2014; mal age difference between each individual with ASD and Nowicka et al. 2016). If difficulties in remembering the past the matched control subject was ± 8 months. In the ASD and disrupted self-referential processing are typical for ASD group, the mean age was 24 years and 4 months. In the (for review see: Lind 2010), one may expect that process- control group, the mean age was 24 years and 2 months. ing of the past self is atypical in this group. In the typically Results of statistical comparisons (both independent- and developing (TD) population, the neural underpinnings of paired-samples t-tests) of the age and IQ (full, verbal, non- processing temporally-distant selves have often been investi- verbal) in the two groups (ASD and TD) are included in gated using the self-reflection task, i.e. evaluation of whether description of Table 1. some personality traits are suitable to describe one’s own All subjects had normal or corrected-to-normal vision person (D’Argembeau et al. 2008, 2010; Luo et al. 2010; and did not take any medication at the time of the experi- Kotlewska and Nowicka 2016). On a behavioral level, a very ment. Subjects were financially compensated for their recent study reported that teenagers with ASD presented participation. reduction in the retrieval of personality traits, poorer knowl- The study conforms to the World Medical Association edge about the self and others and impairment in mental- Declaration of Helsinki. The experiment was undertaken izing abilities (Robinson et al. 2017). In addition, a growing with the understanding and written consent of each sub- body of evidence indicates differences between ASD and ject, and the experimental protocol was approved by the TD groups in the self-referential attribution capacities (e.g. local Ethics Committee (University of Social Sciences and Williams 2010; Woods 2012). However, to the best of our Humanities, Warsaw, Poland). knowledge, there is no study on individuals with ASD that has focused on the neural correlates associated with the pro- cess of reflection in reference to the present and past selves. MRI Acquisition Accordingly, we designed a fMRI experiment aimed at verifying the hypothesis of an impaired process of attribu- MRI data acquisition took place at the Laboratory of tion related to the past self in individuals with ASD. The Brain Imaging, Neurobiology Center, Nencki Institute of two other targets of reflection were the present self and a Experimental Biology on a 3-Tesla MR scanner (Siemens close-other. Based on the numerous fMRI studies, reporting Magnetom Trio TIM, Erlangen, Germany) equipped with atypical self-referential processing reflected in altered acti- a 32-channel phased array head coil. vation of the temporoparietal junction (TPJ), superior tem- Functional data were acquired using a T2*-weighted poral sulcus (STS), cingulate cortex (CC), medial prefrontal gradient echo echo-planar imaging (EPI) sequence with cortex (MPC), and precuneus (e.g. Lombardo et al. 2011; the following parameters: time repetition = 2190 ms, Kestemont et al. 2016), we expected to observe differences time echo = 30 ms, flip angle = 90°, in plane resolu- between individuals with ASD and control subjects in acti- tion = 64 × 64 mm, field of view = 192 mm, and 33 axial vations of the aforementioned brain regions during assign- slices with 3.6 mm slice thickness with no gap between ment of trait adjectives to one’s own person in the past. 1 3 Journal of Autism and Developmental Disorders Table 1 Characteristics of the ASD TD ASD and TD groups Subject Age IQ ADOS Subject Age IQ Full Verb Non-verb Communic Social Int Full Verb Non-verb A1 22:4 106 109 103 3 6 C1 22:1 116 130 97 A2 21:6 106 116 93 3 8 C2 22:3 119 124 110 A3 22:9 97 108 83 6 6 C3 22:2 105 108 103 A4 21:11 117 125 107 3 7 C4 21:11 128 130 123 A5 21:7 102 96 109 5 8 C5 21:7 89 86 93 A6 25:5 108 97 121 4 2 C6 25:9 121 116 126 A7 27:2 111 124 93 2 5 C7 26:10 118 111 126 A8 26:3 86 100 69 3 3 C8 26 97 99 93 A9 22:2 93 96 90 5 8 C9 22:9 101 99 104 A10 27:4 128 143 107 3 7 C10 26:7 132 139 122 A11 24:1 116 114 118 3 3 C11 24:7 127 126 119 A12 28:1 108 112 101 8 4 C12 28:4 110 107 114 A13 27:3 115 116 109 3 5 C13 27:8 123 123 117 A14 24:2 105 110 97 5 8 C14 24:10 115 131 122 A15 21:3 95 100 90 3 9 C15 21:8 110 123 97 Age (years:months), IQ scores for both groups (full—full scale, verb—verbal scale, non-verb—non-verbal performance scale), and ADOS scores for individuals with ASD (communic—communication, social int— social interaction) The independent-samples t-test indicated that age difference was non-significant (P = 0.897). In the case of IQ, between-group difference reached the level of statistical significance (P = 0.043). It turned out that this effect was driven by IQ differences in non-verbal IQ (P = 0.019) and not the verbal one (P = 0.268). The paired-sample t-test also indicated no significant group differences in age (P = 0.350). In the case of IQ levels, between-group difference was significant in reference to the full scale (P = 0.001) and the non-verbal scale (P = 0.003). The between-group difference in verbal IQ scale did not reach the level of statistical sig- nificance, however, a weak trend was found (P = 0.076). In the light of verbal demands of our behavioral task, a lack of differences between the ASD and control group in verbal IQ may support our opinion that between-group differences in fMRI findings were not related to differences in verbal IQ slices. Detailed anatomical data of the brain were experimental conditions as defined by the target of reflec- acquired with a T1-weighted (T1w) MP-RAGE (time rep- tion/evaluation: Present-Self, Past-Self, Close-Other. Within etition = 2530 ms, time echo = 3.32 ms) sequence. Head each block, in turn, event-related design was used. Using movements were minimized with cushions placed around event-related design in each block enabled us to select trials the subjects’ heads. with ‘yes’ responses. This was important as we were inter- ested in separating trials with attributes judged as suitable Stimuli and Experimental Design to describe a given target of reflection/evaluation (present- self, past-self, close-other). There is no doubt that the self- The experimental procedure was prepared in Presentation® referential processing occurred in trials with ‘yes’ responses software (Neurobehavioral Systems, Inc., Albany, CA). as confirmatory responses provided a very clear indication Stimuli were presented centrally on a 21″ MR-compatible that participants were confident about their personal char - LCD screen located in the back of the MR room. Subjects acteristics in the specified time-period (at present, in the viewed the stimuli through an angled mirror attached to the past). A similar approach (i.e. splitting the data based on head coil. whether adjectives were judged as self-descriptive or non- The set of stimuli consisted of adjectives referring to per- self-descriptive) was used in some previous studies (e.g. sonal characteristics (half positive, half negative), the major- Zhang et al. 2013). ity of which were selected from Anderson’s list (Anderson Each block consisted of 72 events/trials during which 1968) and translated into Polish. Adjectives were written in adjectives describing personal features were presented. In white capital letters against a gray background. each trial an adjective was displayed for 3.5 s, followed The experimental paradigm used a mixed block and event by a fixation cross presented for 1 s. Adjectives were pre- related design. A mixed-block design allowed to separate sented in pseudo-randomized order. In each condition, 1 3 Journal of Autism and Developmental Disorders different sets of adjectives were presented. The assign- fMRI Data Analysis ment of lists to experimental conditions was counter- balanced on the group level. Statistical Parametric Mapping (SPM12b, Wellcome Trust A detailed instruction was applied prior to each block Center for Neuroimaging, London, UK) running on MAT- to help the subjects enter a state of reflection about LAB R2013b (The Math-Works Inc. Natick, MA, USA) was the particular person (present-self, past-self, close- used for data preprocessing and statistical analyses. First, other). Additionally, one of the question was presented functional images were motion corrected (head movements between sub-sets of 24 stimuli: “Are you…”; “When you were < 4 mm in all cases, with no significant differences in were about 14, were you…”; “Is your father (/brother/ movements between groups). Then, structural images from friend)…”. Subjects were tasked with judging whether single subjects were co-registered to the mean functional a given adjective was suitable to describe/characterize image. The functional images were normalized to MNI a person specified in the instruction in a single block space using compositions of flow fields and group-specific (present-self, past-self, close-other). Yes/no responses template to a 2 mm isotropic voxel size. Finally, the normal- were given by pressing one of two buttons on a response ized functional images were smoothed with 6 mm isotropic pad. In the subsequent analyses of behavioral and fMRI Gaussian kernel. data only trials with ‘yes’ responses were included (the In the first-level of statistical analysis, all experimental ‘no’ responses would add some ‘noise’ to the analyzed conditions and head movement (translation and rotation) BOLD signal). Each block lasted approximately 6 min. parameters were entered into the design matrix. The data Participants were asked to freely choose their Close- were modeled for each of the three experimental fMRI runs Other among the persons who were the most significant to and using the canonical hemodynamic response function the participant ‘at present’, i.e. at the time of our experi- convolved with the experimental conditions (present-self, ment, with the only restriction: the gender should be the past-self, close-other). The model included only the events same as the gender of our participants, i.e. male. This was that were positively categorized (i.e. ‘yes’ responses were done to avoid a situation in which a pre-defined person given) to a relevant experimental condition separately by is not really close to a particular subject; and also we each subject. wanted to avoid different grammatical forms of adjec- The following single t-tests were computed at 1st level tives used to describe females in Polish. Thus, prior to (within subject): present-self, past-self, and close-other. In the fMRI study participants were requested to assign a the 2nd level (between subject) analysis, a flexible facto- closely-related person, and describe their relationship rial design was used with intergroup factor ASD vs. con- briefly. Only 3 control subjects chose their close-friend trol and within group factor ‘condition’ (present-self vs. and a vast majority of the subjects (27) chose their father past-self vs. close-other). Additionally, for the all-subject or brother (ASD group: 12—father; 3—brother; control analysis (ASD + TD) a full factorial design was used for group: 7—father; 5—brother). statistical calculation of the within-group factor ‘condi- Moreover, the past self was defined as ‘the self in mid- tion’: present-self—fix (fixation cross) vs. past-self—fix vs. dle high school.’ Therefore, in the past-self condition close-other—fix. our subjects were asked to ‘mentally move’ to the time On a group level a voxel-wise height threshold of when they attended middle high school. As our subjects P < 0.001 (uncorrected) combined with a cluster-level extent were about 24 years old, such ‘past self’ seemed to be threshold of P < 0.05 (cluster size > 30 voxels; corrected for well-defined and appropriate for investigation of the self multiple comparisons using the family wise error (FWE) across time (D’Argembeau et al. 2008, 2010; Kotlewska rate) was employed for whole brain analyses. and Nowicka 2016). MNI coordinates were translated to Talairach space using Before the experimental MRI session, each subject GingerALE software (http://www.brainmap.or g). Talairach- took part in a training session in a mock MRI scanner Client 2.4.2 was then used to identify the activated structures situated in the Laboratory of Brain Imaging. The train- (Lancaster et al. 2000; http://www.talai rach.org). ing session was performed between 1 week and 1 day prior the experimental session. During the training ses- sion shorter stimuli sets were used, with different stimuli Results sequences and different assignment of adjectives lists to experimental conditions. The training session aimed at Behavioral Results familiarizing ASD subjects with the MRI environment. Control subjects underwent the same training procedure Table 2 presents the mean raw numbers and mean relative in order to equalize the experimental experience of both percentages of positive and negative adjectives assigned groups. to each experimental condition: present-self, past-self, 1 3 Journal of Autism and Developmental Disorders Table 2 Behavioral results: mean raw numbers, mean relative per- No significant effects were found in the ‘present-self’ and centages and their standard deviations (in brackets) of positive and ‘close-other’ conditions (see Table 2). negative adjectives assigned by ASD and TD groups to each experi- mental condition: present-self, past-self, close-other fMRI Results Condition Positive adjectives assign- Negative adjectives assign- ments ments Eec ff ts for ASD + TD Subjects ASD TD ASD TD Analyses for the two groups collapsed together (ASD + TD Present- 23.5 (7.1) 23.6 (5.3) 12.0 (5.8) 10.1 (3.8) group) revealed main effect of task with clusters of signifi- self 65.3% 65.6% 33.3% 28.1% (10.6) (19.7) (14.7) (16.1) cant activity for all analyzed contrasts (‘present-self—fix’, Past-self 18.6 (5.2) 22.0 (4.5) 14.6 (8.8) 12.7 (6.6) ‘past-self—fix’, ‘close-other—fix’). For all conditions 51.7% 61.1% 40.6% 35.3% (18.3) taken together we found a number of cortical structures (14.4) (12.5) (24.4) that revealed positive contrast values (see Table 3; Fig. 1a), Close-other 24.4 (5.7) 23.3 (3.3) 7.9 (6.3) 9.6 (5.0) including: the middle cingulate gyrus—MCG/precuneus 67.8% 65.6% (9.2) 21.9% 26.7% (13.9) (T = 12.94; 4187 voxels), right middle frontal gyrus—MFG (15.8) (17.5) (T = 6.13; 169 voxels), anterior cingulate gyrus—ACG (T = 4.66; 109 voxels), left insula (T = 6.5; 237 voxels), right close-other by individuals with ASD and control subjects. insula (T = 5.70; 87 voxels) and right inferior frontal gyrus— The number of omitted trials was very low in each group IFG (T = 4.9; 56 voxels). However, there were no significant (mean number: 1.4 and 0.36 for ‘present-self’, 1.0 and 0.16 differences between specified contrasts. for ‘past-self’, and 1.13 0.2 for ‘close-other’, in the ASD and control group, respectively). It did not differ neither Eec ff ts for the ASD Group vs. the TD Group between groups nor conditions (all Ps > 0.290). Analysis of ‘yes’ responses with group and experi- First, for all experimental conditions (present-self, past-self, mental condition as factors revealed no significant main close-other) collapsed together, we found positive differ - effects or interactions. However, between-group statistical ences between ASD and TD groups in contrast estimates in comparisons—performed separately for each experimental response to adjectives that were selected by the subjects as condition—for the number of positive and negative attrib- descriptive for each of the specified conditions. Significantly utes assigned by individuals with ASD and control sub- stronger activations in the ASD group were observed in one jects showed that in the ‘past-self’ condition, significantly structure—the right posterior superior temporal gyrus— more positive attributes were ascribed by control subjects STG (T = 5.08; 30 voxels). Interestingly, the additional than by individuals with ASD (F = 4.462; P = 0.044). analysis revealed that the cluster of enhanced activation in 1,28 ASD subjects was wider when the ‘present-self’ condition Table 3 fMRI results: Structure Group/condition Peak coordinates P (FWE- significant activations with x, y, z corrected) peak Talairach coordinates and P-values MCG/precuneus ASD + TD/all conditions 12, − 39, 42 0.0001 Right MFG 29, 28, 49 0.0001 ACG 5, 42, 0 0.0001 Left insula − 38, − 18, − 4 0.0001 Right insula 36, − 4, − 14 0.002 Right IFG 40, 39, 14 0.01 Right STG ASD > TD/all conditions 50, − 21, 14 0.029 Right STG ASD > TD/‘past-self’ 54, − 21, 0 0.0001 Right TPJ 54, − 49, 7 0.047 PCG/left cuneus − 13, − 70, 7 0.0001 Left MTG/STG − 59, − 14, − 4 0.0001 Left posterior STG/TPJ − 59, − 46, 11 0.007 Right insula 33, − 21, 14 0.0001 ASD Autism Spectrum Disorder group, TD typically developing group, MCG middle cingulate gyrus, MFG middle frontal gyrus, ACG anterior cingulate gyrus, IFG inferior frontal gyrus, STG superior tempo- ral gyrus, TPJ temporoparietal junction, PCG posterior cingulate gyrus, MTG middle temporal gyrus 1 3 Journal of Autism and Developmental Disorders Fig. 1 Results of fMRI analysis. a Results of contrast analysis for standard deviations of group-level contrast estimates for each of the all participants (ASD + TD) and all conditions (‘self’ + ‘past-self’ + clusters of significant activity. Lower graph presents mean values of ‘close-other’) together. The graph placed below brain images present percent signal change for each of the clusters of significant difference mean values and standard deviations of group-level contrast estimates in activity between ASD and TD group. r right, l left, p posterior, for each of the clusters of significant activity. b Results of between MCG middle cingulate gyrus, Precun. precuneus, MFG middle fron- group comparison (ASD > TD) for ‘past-self’ condition. In both tal gyrus, ACG anterior cingulate gyrus, IFG inferior frontal gyrus, panels regions of significant contrasts (FWE-corrected at the cluster STG superior temporal gyrus, TPJ temporoparietal junction, PCG level, P < 0.001; cluster size > 30 voxels) are plotted (red color) on posterior cingulate gyrus, MTG middle temporal gyrus. (Color figure the template of grey matter tissue probability map (TMP.nii, SPM12). online) The upper graph placed below brain images presents mean values and 1 3 Journal of Autism and Developmental Disorders was excluded from the analysis. The comparison of ‘past- the TD group. On the other hand, both groups presented self’ and ‘close-other’ taken together revealed larger cluster similar positivity bias in the case of present self and the of increased activity in the ASD group in the same region close-other conditions. of STG/TPJ (T = 5.14; 107 voxels). We found no regions of On the neural level, fMRI results for both groups of significantly stronger activity in TD group vs. ASD group. subjects collapsed together showed significant activations Secondly, inter-group comparisons were done for each in MCG, ACG, Insula, and MFG, typically reported for experimental condition (present-self, past-self, close-other). self-related information processing and mentalizing (e.g. Significant clusters of enhanced activation in individuals Lombardo et al. 2011; Murray et al. 2012; Kestemont et al. with ASD were found only in the case of the past-self con- 2015) as well as for reflection on present and past selves dition. Such atypical activity was observed in right insula (D’Argembeau et al. 2008). In addition, we found activa- and right STG (T = 4.70; 177 voxels), right TPJ (T = 4.26; tions in the right IFG and precuneus that were previously 38 voxels), posterior cingulate—PCG/cuneus (T = 4.54; 344 reported specifically in the case of self-reflection across time voxels), left middle temporal gyrus—MTG/STG (T = 4.39; (D’Argembeau et al. 2008). However, we did not found sig- 102 voxels) and left posterior STG/TPJ (T = 4.27; 63 voxels) nificant differences in brain activation between self-related (see Table 3; Fig. 1b). For all analyzed experimental condi- and other person-related conditions. It is worth noting that in tions we found no cortical regions of significantly stronger the current study, we compared brain activity during evalu- activity in TD vs. ASD group. ation of the self with the close-other—not like in many of the previous studies with a famous (e.g. Kelley et al. 2002) or familiar but not personally known person (Pfeifer et al. Discussion 2007, 2013a). As it has been already shown, this distinc- tion is important for the extent of differences between brain A critical aspect of self-related cognition is the ability to responses for the self and other. The areas of activity are remember events that occurred in one’s past (McAdams highly common if the other is personally known, very sig- 2001; Conway 2005). It has been suggested that difficul- nificant person (Kennedy and Courchesne 2008; Tacikowski ties in accessing specific autobiographical memories in et al. 2013; Laurita et al. 2017). A lack of differentiation ASD may be due to problems in using the self as an effec- between the self and the other in cortical midline structures tive memory organizational system (Crane et al. 2009). In (CMS) has been observed in prior studies, most frequently a study examining narratives of self-defining and every - when targets of ree fl ction were either very close or similar to day autobiographical memories in adults with ASD, it was the self (Ochsner et al. 2005; Krienen et al. 2010). Interest- shown that individuals with ASD extracted less meaning ingly, results of one of the studies on self-processing, where from their memories than adult controls, which may be inter- close friend was included as a condition in an evaluative preted as a failure in using past experiences to update the perspective task, revealed the differences in brain activity self (Crane et al. 2010). However, no previous studies have between self and other person conditions only in the group examined the temporally-distant selves in ASD using a task of adolescents and not in the group of adults (Jankowski other than memory tasks. et al. 2014). It is also worth noting that in our study the con- In the present fMRI study, we investigated the neural cor- trasts for conditions were made for both groups ASD and TD relates of adjectives (referring to personal features) assign- collapsed together. Therefore, the effects specific for ASD ment to the present self, the past self, and a personally- group may bias our comparisons resulting in less typical relevant person in high functioning individuals with ASD. activation patterns that had not been reported in previous During fMRI scanning subjects were required to evaluate research on general population. Specifically, it was previ- whether adjectives were suitable to describe their person at ously shown that in contrast to TD groups, CMS activations present, their person in the past (at the time of middle high in individuals with ASD were similar for the self and other school), and a close-other (friend or family member). The set (e.g. Kennedy and Courchesne 2008) or even stronger for of adjectives for each target of reflection included an equal- other than the self condition (Lombardo et al. 2010). ized number of positive and negative features. Moreover, analysis of fMRI data revealed differences On the behavioral level, no significant between group between the ASD and TD groups that were common for effects were found while analyzing all experimental con- all experimental conditions (present-self, past-self, close- ditions together (present-self, past-self, close-other). How- other) collapsed together. During the attribution process ever, analyses done for each condition separately revealed ASD subjects exhibited elevated activity in one cortical significant inter-group differences in the number of positive structure—the right posterior STG/TPJ. Interestingly, fur- attributions made while evaluating personal features of the ther exploration of this result suggested that this stronger past self. In this case, individuals with ASD presented sig- activity was driven mainly by the inter-group difference in nificantly weaker positivity bias (Mezulis et al. 2004) than two of the analyzed conditions—past-self and close-other. 1 3 Journal of Autism and Developmental Disorders Finally, analyses done for each condition separately showed suggest the need for involvement of some additional brain significantly stronger activation in individuals with ASD resources by subjects with ASD to process more ambigu- when compared to TD group in the ‘past-self’ condition in a ous social information. It was previously proposed that number of brain regions: the right insula, PCG, right and left hyperactivity of the STS/TPJ may reflect the engagement posterior STG/TPJ, and left MTG. Importantly, percent sig- of those areas that are involved in a more general cogni- nal change measures suggest that the inter-group differences tive processing which compensate for impairments in attri- in all of those regions are driven by the enhanced activity bution judgements (Kestemont et al. 2016). In our study, among ASD subjects and diminished activity in TD group. apart from the right TPJ—the structure consequently linked The effect observed in the ASD group during retrieval to mentalizing abilities—we found activity in neighbor- of personal attributes about the past self could not be ing areas of the STS/STG and MTG. In previous research, directly related to previous findings, as none of the earlier those structures were linked to recognition of other people’s fMRI studies on ASD investigated the neural mechanisms intentions mainly based on their body and gaze movement, underlying reflection on personal features of the past self. and had direct connections with the mentalizing networks Nevertheless, there are some important links between our (Pelphrey et al. 2011). Importantly, activations in TPJ and results and the published literature. For example, in a very adjacent posterior STG, found in the ASD group, may be recent fMRI study that included subclinical and clinical also linked to reflected self-appraisals—a task involving ASD groups, subjects were engaged in a causal attribution mentalizing processes (Pfeifer et al. 2009; Pfeifer and Peake task that included self, another person, and situation condi- 2012). Although our participants were not instructed to think tions. Similarly to our findings, hyperactivity in the neural about other people’s perspectives on the self, they seemed to network including the posterior STS and TPJ was reported activate components of the social perception network includ- in individuals with ASD (Kestemont et al. 2016). Our results ing TPJ and posterior STG (Pfeifer et al. 2009, 2017). It are also in line with several previous studies that revealed was previously shown that neuro-typical adolescents when stronger activity or diminished task selectivity of relevant compared to adults during both direct and reflected self- brain structures during performance of mentalizing about appraisals more extensively engage brain regions involved self and others (e.g. Mason et al. 2008; Lombardo et al. in perspective-taking, like TPJ (Pfeifer et al. 2009). This 2011; Schulte-Rüther et al. 2011). may suggest a delayed development of cognitive networks Importantly, we observed atypical processing of informa- involved in the past self processing in examined adult ASD tion related to the past self on both the behavioral and neural subjects. It may be also hypothesized that in individuals with levels. Behaviorally individuals with ASD were less inclined ASD their characteristic of the past self is based to a higher than their TD counterparts to assign positive attributes to extent on information received from social environment (e.g. their own person in the past. It was previously shown that TD family members, therapists) than on the internalized knowl- youths make more positive self-appraisals than youths with edge about themselves. The later notion, however, is highly ASD during self-evaluation tasks (Pfeifer et al. 2013b). ASD speculative in nature. children were also characterized by diminished preference Additionally, we found a cluster of increased activity in for memorizing positive over negative adjectives when those our ASD group that included the very posterior part of the attributes had to be referred to themselves (Burrows et al. cingulate gyrus and cuneus. Activity in this area may sug- 2017). Moreover, in our study the ASD group was character- gest the involvement of imagery and memory of concrete ized by broad activity mainly in the posterior brain regions episodic events using visual representations during retrieval while reflecting on the past self. Importantly this extended of past self attributes (e.g. Addis et al. 2004). This enhanced network of activity includes areas that were disengaged in activation of posterior brain regions found in the ASD group the TD group in the past-self condition. These results reflect may also indicate that individuals with ASD seem to be ‘vis- highly atypical pattern of brain regions involved in retrieval ual thinkers’ (Grandin 2009), i.e. individuals with ASD may of autobiographical memory and self-characteristics from tend to visualize one selves in the past in order to be able to the past in individuals with ASD. We hypothesize that describe/characterize themselves in the past. stronger activations in the past-self condition observed in All in all, findings of the current study may suggest individuals with ASD may reflect the higher—in comparison that in our study individuals with ASD recruited addi- to control subjects—level of difficulty of reflecting on one’s tional areas to engage imagination and more embodied own person in the past. This notion is based on numerous representations of their own behaviors and intentions from studies showing that the more difficult the task the stronger the past, which were crucial for recollection of personal and/or larger the activations (e.g. Gould et al. 2003; Erickson traits describing the past self. They may also refer to the et al. 2007; Nowicka et al. 2011). information about their past characteristics received from In line with the latter, enhanced engagement of right and their social environment to a higher extent than the TD left posterior temporal regions and parts of the TPJ may adults. Thus, recruitment of additional areas may serve 1 3 Journal of Autism and Developmental Disorders as a kind of a compensatory mechanism for abnormalities Finally, we would like to comment on the limitations in autobiographic memory reported among subjects with of the present study. First of all, the study is confined by ASD (Brezis 2015). a small sample size. Thus, the reported results should be While significant inter-group differences were found in treated with caution and they need to be further investi- the past-self condition, they were absent in the present-self gated in larger groups of individuals with ASD in order conditions. This may also be viewed in the light of research to enhance statistical power. Secondly the experimental on autobiographical memory in ASD. Studies on episodic group was limited to high functioning adult males. There- autobiographical memory for different periods in subjects’ fore our behavioral and brain imaging results could not lifetimes found that in ASD memories for recent events were be generalized to all individuals with ASD, irrespective more specific and detailed than for remote events (Bruck of sex. Moreover, as they were high functioning individu- et al. 2007; Crane and Goddard 2008; Tanweer et al. 2010; als, there is a possibility that the alternative strategies of Goddard et al. 2014). Thus, one may assume that assignment activation of brain areas that they showed in this study of adjectives to one’s own person at present was much easier would be different from those detectable in low function- than to the self in the past; the latter forced individuals with ing persons with autism. In addition, a higher number of ASD to ‘mentally move’ to their far past in order to judge experimental trials/events focused on mechanisms of past whether some traits were suitable to characterize their per- self-processing would also be beneficial; this would ena- son while attending middle high school. There is rather no ble more detailed investigation of effects related to—for doubt that this task can be characterized as episodic autobio- instance—positive and negative adjectives that could be graphical memory. However, one may speculate that depend- detected in fMRI data. Moreover, it would be worth to ing on the trait presented to participants, their personal include present and past aspects of the close-other into experience and their self-awareness, they may sometimes experimental design of future studies in this field. We refer also to their semantic knowledge. The reason is that propose that in such case the close-other should be pre- some of the personal characteristics are rather stable over defined as a friend that had been the friend since the time time (e.g. intelligent, blond) and other not necessarily (e.g. of attending a high school. As a consequence, the defini- responsible, tall). Therefore, we assume that semantic and tion of past self and past close-other would be the same episodic memory may be interactively engaged, if a subject and participants would be required to refer to their and the could not retrieve his specific characteristic in the past and close-other’s personal characteristics at present and during had to ‘mentally move’ to the past situations using episodic the same time period in their past. This approach would memory. enable comparisons that may reveal additional inter-group Our supposition is directly supported by fMRI findings differences associated with processing of information of the present study, i.e. stronger activation of posterior about the distant past. brain regions, including the PCG and bilateral temporal Acknowledgments This work was supported by the National Science areas in the ASD group. Importantly, numerous previous Centre, Poland (Grant PRELUDIUM, UMO-2014/13/N/HS6/02613 studies have linked those structures with both episodic and to HBC). We thank all participants and families of participants in the semantic autobiographic memory retrieval (for meta-anal- ASD group. We also thank Michał Wroniszewski, Joanna Grochowska, and Urszula Wójcik from the SYNAPSIS Foundation for their help in ysis see: Martinelli et al. 2013). Martinelli et al. proposed selecting the groups of participants, and Izabela Chojnicka for her help to include the conceptual self as one of the components of in ADOS assessments. autobiographic memory that specifically relates to abstract self-representation and personal traits identified and inter - Author Contributions HBC planed and designed the study, ran the nalized across the lifespan experience. However, the con- experiment, analyzed and interpreted the data and drafted the manu- ceptual self was specifically related to activity in the fron- script; AM participated in the design and coordination of the experi- ment was involved in the data analysis and helped to draft the manu- tal brain structures (Martinelli et al. 2013). Importantly, in script; IK participated in the design and execution of the experiment the present study frontal cortical structures were not found and helped to draft the manuscript; AN participated in the design of among clusters of significantly stronger activity in individu- the study, interpreted the data and drafted the manuscript. All authors als with ASD. read and approved the final manuscript. In conclusion, we propose that the specific difficulties observed in the ASD group in attributing personal traits Compliance with Ethical Standards to the past self resulted in extensive engagement of neural Conflict of interest The authors declare no conflict of interest. mechanisms related mostly to the semantic and/or episodic components of autobiographic memory (Crane and Goddard Ethical Approval All procedures performed in studies involving human 2008; Brezis 2015), with additional components of imagery participants were in accordance with the ethical standards of the insti- tutional and/or national research committee and with the 1964 Helsinki (e.g. Addis et al. 2004) and embodied representations of the declaration and its later amendments or comparable ethical standards. past events and facts (Pelphrey et al. 2011). 1 3 Journal of Autism and Developmental Disorders Open Access This article is distributed under the terms of the Crea- D’Argembeau, A., Stawarczyk, D., Majerus, S., Collette, F., Van der tive Commons Attribution 4.0 International License (http://creat iveco Linden, M., Feyers, D., Maquet, P., & Salmon, E. 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