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Brain Structure Links Loneliness to Social Perception

Brain Structure Links Loneliness to Social Perception Current Biology 22, 1975–1979, October 23, 2012 ª2012 Elsevier Ltd. Open access under CC BY license. http://dx.doi.org/10.1016/j.cub.2012.08.045 Report Brain Structure Links Loneliness to Social Perception 1, 1,2,3 4 Ryota Kanai, * Bahador Bahrami, Brad Duchaine, the pSTS cluster (Figure 1). The peak voxel was situated within 5 1,5 1,2 Agnieszka Janik, Michael J. Banissy, and Geraint Rees the middle temporal gyrus (T[103] = 4.66, Z = 4.42, R = 0.174, UCL Institute of Cognitive Neuroscience, 17 Queen Square, p[FWE-corr] = 0.02, MNI coordinate x = 248, y = 269, z = 15). London WC1N 3AR, UK We did not find any significant cluster that positively correlated Wellcome Trust Centre for Neuroimaging, Institute of with loneliness (p[corr] > 0.05 nonstationary correction; see Neurology, University College London, 12 Queen Square, Table S1 available online for uncorrected results). London WC1N 3BG, UK Given the known functions of pSTS in social perception Interacting Minds Project, Institute of Anthropology, [16, 17], it appears unlikely that the volume of the left pSTS Archaeology, Linguistics, Aarhus University, and Centre of directly mediates subjective experiences of loneliness per Functionally Integrative Neuroscience, Aarhus University se. The pSTS region is thought to be involved in initial stages Hospital, Norrebrogade 44, Building 10 G, of social perception combining different sensory cues such 8000 Aarhus C, Denmark as eye gaze, hand action, and body movements [16]. In partic- Department of Psychological and Brain Sciences, Dartmouth ular, the position of the pSTS cluster revealed in our VBM result College, Moore Hall 6207, Hanover, NH 03755, USA is close to the locus where activations are elicited when Department of Psychology, Goldsmiths, University of viewing the eye gaze of others [18]. Specifically, our pSTS London, New Cross, London SE14 6NW, UK locus overlapped with the mean coordinate of the loci sensi- tive to eyes (x = 248, y = 255, z = 6; see [16] for a meta- analysis). Summary Experiment 2. Social Perception and Loneliness Loneliness is the distressing feeling associated with the Taking our findings from experiment 1 with the previously perceived absence of satisfying social relationships [1]. established functional role of pSTS leads to the intriguing Loneliness is increasingly prevalent in modern societies hypothesis that lonely individuals might have deficits in basic [2, 3] and has detrimental effects on health and happiness social perception. [4, 5]. Although situational threats to social relationships We tested this hypothesis in a subset of the original partici- can transiently induce the emotion of loneliness, suscepti- pants (n = 22) using a gaze perception task. Participants were bility to loneliness is a stable trait that varies across individ- shown three faces and asked to judge which face showed uals [6–8] and is to some extent heritable [9–11]. However, strabismic gaze (eyes not aligned properly). We found that little is known about the neural processes associated with the ability to process eye gaze information was negatively loneliness (but see [12–14]). Here, we hypothesized that correlated with self-reported loneliness (Figure 2A; R = 20.51, individual differences in loneliness might be reflected in T[20] = 22.64, p = 0.015). We replicated this association in an the structure of the brain regions associated with social independent sample (n = 38) using a more naturalistic gaze processes [15]. To test this hypothesis, we used voxel-based task and confirmed the specificity of this association, because morphometry and showed that lonely individuals have less it was not observed for a nonsocial face perception task (see gray matter in the left posterior superior temporal sulcus Experiment S1 and Figure S1). Moreover, the efficiency of (pSTS)—an area implicated in basic social perception. As eye gaze processing was significantly correlated with the this finding predicted, we further confirmed that loneliness regional gray matter volume of the pSTS cluster (Figure 3A; was associated with difficulty in processing social cues. R = 0.441, T[20] = 2.21, p = 0.038). Although other sociopsychological factors such as social Although the results so far suggest that pSTS, eye gaze pro- network size, anxiety, and empathy independently contrib- cessing, and loneliness are linked with one another, whether uted to loneliness, only basic social perception skills the gaze perception ability mediates the relationship between mediated the association between the pSTS volume and the volume of pSTS and loneliness remained uncertain. We loneliness. Taken together, our results suggest that basic therefore computed the partial correlation between pSTS social perceptual abilities play an important role in shaping volume and loneliness while regressing out the contribution an individual’s loneliness. of eye gaze performance. This revealed that the original sig- nificant correlation between pSTS gray matter volume and loneliness in this sample (R = 20.454, p = 0.03) vanished after Results controlling for individual differences in eye gaze performance (R = 20.138, p = 0.550). This supports the notion that the Experiment 1. Voxel-Based Morphometry of Loneliness negative correlation between pSTS volume and loneliness We correlated brain structure and reported loneliness in a was mediated by the efficiency of perceiving eye gaze. sample of 108 healthy adults (see Experimental Procedures) To examine whether the relationship between loneliness and and found a large significant cluster in the posterior superior social perception via pSTS was specific to eye gaze per- temporal sulcus (pSTS) in which the regional gray matter ception, we examined participants’ abilities on several other volume negatively correlated with individual differences in types of social perception tasks, namely, facial expression loneliness (cluster size = 3,837 mm , p[corr] < 0.05 nonsta- discrimination [19, 20], facial identity discrimination [19, 20], tionary). Lonely individuals had smaller gray matter volume in and facial emotion recognition [20, 21]. The correlation between loneliness and the ability to discriminate facial *Correspondence: [email protected] emotional expressions did not reach statistical significance Current Biology Vol 22 No 20 of the original participants (n = 45). We found that although social network size was strongly correlated with the loneliness scale (R = 20.617, T[43] = 25.144,p < 0.001), factoring out the social network scale did not affect the pSTS-loneliness corre- lation (R = 20.395, T[42] = 22.789, p = 0.008; original correla- tion in this sample, R = 20.386, T[42] = 22.743, p = 0.009). There was also no correlation between pSTS size and the social network scale (R = 0.125, T[43] = 20.823, p = 0.413), because the overlap between the pSTS cluster for loneliness the cluster previously reported for online social network size overlapped only less than 1% (see Figure S2). These results together indicate that the left pSTS gray matter volume and social network size independently predict an individual’s loneliness. Experiment 4. Trait Anxiety and Loneliness Loneliness scores are correlated with other mood factors such as anxiety and depressive symptoms [23]. To examine whether such mood measures mediated the association between the volume of pSTS and loneliness, we administered the STAI inventory to collect data on trait anxiety from 61 of our original participants in experiment 1. We replicated previous findings [23] showing that trait anxiety is highly correlated with loneliness score (R = 0.596, p < 0.001). We extracted the pSTS volume from MRI scans of this subpopulation of participants and found that trait anxiety also showed a tendency to negatively correlate with Figure 1. Gray Matter Volume Correlated with Loneliness Scale pSTS volume, but this did not reach statistical significance (A) The left STS in which variability in gray matter volume exhibited signifi- (R = 20.226, p = 0.08). Because this subpopulation was cant negative correlation with loneliness scale (n = 108) is superimposed selected from the participants in experiment 1, we observed on a standard T1-weighted template brain in MNI stereotactic space. The the expected negative correlation between loneliness score significant cluster is shown at t > 2.3 for visualization purpose. (B) A scatterplot between loneliness scale and pSTS volume adjusted for and pSTS volume in this subsample (R = 20.596, p < 0.001). age, gender, and total gray matter volume is shown for illustration purpose To examine whether this correlation was (partially) mediated only. Statistical inference was based on the p value corrected for multiple by trait anxiety, we tested whether the correlation was weak- comparisons across the whole brain at a cluster level with nonstationary ened by inclusion of anxiety as a covariate. However, the lone- correction [44]. liness-pSTS correlation was unaffected by regressing out the contribution of anxiety (R = 20.568, p < 0.001). These results (Figure 2B; R = 20.376, T[20] = 21.81, p = 0.085). However, indicate that the volume of left pSTS and trait anxiety indepen- this performance was significantly correlated with the gray dently contribute to loneliness score. matter volume in the pSTS cluster (Figure 3B; R = 0.492, T[20] = 2.528, p = 0.020). Similarly, sensitivity to face identity Experiment 5. Empathy and Loneliness did not correlate with loneliness (Figure 2C; R = 20.167, Finally, we examined whether loneliness was associated with T[20] = 20.759, p = 0.457) but significantly correlated with aspects of empathy using the Interpersonal Reactivity Index the gray matter volume in the pSTS cluster (Figure 3C; R = (IRI), which measures fantasy scale (FS), perspective taking 0.544, T[20] = 2.899, p = 0.009). Performance in the emotion (PT), personal distress (PD), and empathic concern (EC) recognition task (measured by efficiency score) did not signif- [24, 25]. We collected these IRI subscales from a subset (n = icantly correlate with loneliness (Figure 2D; R = 0.258, T[20] = 95) of the participants studied in experiment 1. We found 1.19, p = 0.257) or the gray matter volume in the pSTS cluster that the loneliness score significantly correlated with PD (Figure 3D; R = 0.403, T[20] = 1.97, p = 0.063). Taken together, (T[93] = 3.59, R = 0.349, p < 0.01, Bonferroni corrected), but loneliness was correlated with the perception of eye gaze, not with other subscales (FS, T[93] < 1, R = 0.028, p = 0.316; whereas the gray matter volume of the left pSTS correlated PT, T[93] = 21.97, R = 20.200, p = 0.208; EC, T[93] = 22.30, more broadly with processing social cues from faces. R= 20.233, p = 0.092, Bonferroni corrected). This is in line with previous reports that people with a high PD score show Experiment 3. Social Network Size and Loneliness poor social perception and social competence [24] and further Next, we examined whether social network size could explain supports our findings that loneliness is related to reductions in the correlation between loneliness and pSTS. Previously, we social perception. None of these subscales were, however, have shown that the gray matter volume of the middle significantly associated with the volume of the left pSTS (all temporal gyrus (MTG) region abutting the pSTS region associ- p > 0.05). ated with loneliness correlates with online social network size [22]. Thus, it is possible that the link between pSTS and Discussion loneliness was mediated by individual differences in social network size. We therefore examined whether the pSTS- Our experiments show that individual differences in the loneliness correlation could be explained by social network expressed trait of loneliness are linked with variations in size by collecting data on social network size from a subset the gray matter volume of left pSTS. This region has been Loneliness and Social Perception Figure 2. Relationship between Loneliness Scale and Performances for Social Perception Tasks (n = 22) Abnormal gaze detection task (A), same-different emotion discrimination task (B), same-different identity discrimination task (C), and films emotion recognition task (D). See Experimental Proce- dures for full details of the tasks. Specifically, lonely individuals show weaker activation in the ventral striatum when viewing pictures of pleasant social events than when viewing pleasant pictures of nonsocial objects, whereas this pattern is reversed for nonlonely individuals. Furthermore, lonely individ- uals show weaker activations in bilateral temporoparietal junction (TPJ) to unpleasant social pictures of people compared to unpleasant pictures of objects. Although functional and struc- tural correlates of loneliness may be regionally dissociated, both the previous functional study [14] and our current study point to the idea that loneliness is reflected in the way the brain processes visually presented social cues. In future research, conjoint measurements of structure and function will be needed to establish their relationships. implicated in several fundamental aspects of processing The correlation we observed between pSTS and loneliness social information. However, it is unlikely that pSTS directly seems to be specifically mediated by the ability to process (or any other single brain area per se) mediates such a complex eye gaze information, because factoring out the eye gaze performance abolished the correlation between pSTS and cognitive quality as the transient feeling of loneliness. This brain region is causally involved in perception of social stimuli loneliness. This was not observed with other measures such such as biological motion [26, 27] and gaze direction [28], sug- as social network size, anxiety, and empathy (personal gesting that the feeling of loneliness may be associated with distress in particular) that were correlated with loneliness. deficits in these basic social perceptual skills. Our behavioral These results suggest that a multitude of social and psycho- experiments confirmed this hypothesis by showing significant logical factors contribute to loneliness score, but their correlations between individual variability on the reported association with loneliness is independent of the pSTS struc- loneliness scale and objectively measured skills relevant to ture. We speculate that interindividual differences in those social perception such as the performance of eye gaze factors may also have a basis in the structure of other brain perception. Furthermore, the volume of pSTS also predicted regions [22, 25, 36–39], but their associations with loneliness such basic social skills, which confirms the relevance of the may have been too weak to be detected within our current same pSTS region in those social perception tasks. sample size (n = 108). Further investigation with a larger Our findings indicate that lonely individuals have deficits at sample may help reveal more regions that are relevant for individual differences in loneliness. Future studies may benefit a relatively early stage of processing social cues. Lonely indi- viduals are low in social skills [29, 30] and have poor sensitivity from asking participants under what kind of circumstances to nonverbal communication [31], whereas they are proficient they feel lonely, because such qualitative data may help us in verbal communication [32]. People with poor social skills are understand how multiple pathways lead to loneliness in more likely to become lonely when they encounter negative different individuals. stressful life events [33]. This finding is in line with the hypoth- Because of the cross-sectional nature of our present study, esis that social skills deficits are antecedents of loneliness we cannot determine the direction of causation between lone- [34]. However, it should be noted that in those studies, social liness, social perceptual abilities, and the volume of the left skills were measured by different methods such as question- pSTS. One appealing possibility is that poor ability to recog- naires (e.g., the Social Skills Inventory, [35]) and it remains nize social cues may lead to social isolation and loneliness. unclear whether social skills measured by questionnaire items For example, people who are poor at reading social cues (e.g., ‘‘At parties I can instantly tell when someone is interested may experience difficulty in developing social relationships. in me.’’) correspond to basic aspects of social perception This hypothesis predicts that improvements in social percep- measured in the laboratory as here. tion by training may increase the quality and quantity of social Subjective loneliness modulates brain activations to interaction and thereby mitigate the degree of subjective lone- pleasant and unpleasant pictures of other people [14]. liness. A recent meta-analysis of intervention studies that Current Biology Vol 22 No 20 Figure 3. Relationship between Regional pSTS Volume and Behavioral Performances in Social Perception Tasks (n = 22) Abnormal gaze detection task (A), same-different emotion discrimination task (B), same-different identity discrimination task (C), and films emotion recognition task (D). See Experimental Proce- dures for full details of the tasks. and total gray matter volume of individual brains were included in the design matrix as covariates of no interest. We used a threshold of p(corr) < 0.05 corrected for multiple compari- sons at a cluster level using nonstationary correction [44]. Experiment 2. Social Perception and Loneliness We contacted the participants in experiment 1 and asked them to take part in follow-up experi- ments. A total of 22 healthy volunteers (aged 19–30, mean 22.7 6 SD 3.9, 15 females) were tested on four social perception tasks: abnormal gaze detection task, emotional expression dis- crimination task, identity discrimination task, and films emotion recognition task (see Supple- mental Experimental Procedures for full details). Experiment 3. Social Network Size and Loneliness Forty-five participants recruited from the UCL student community (aged 18–30 mean 23.2 6 SD 3.6, 52 females) completed the social network size questionnaire [45]. A normalized aimed to reduce loneliness with various strategies showed social network size was computed for each participant by averaging the Z scores for all the questions items (see Supplemental Experimental that the most effective intervention for treating loneliness is Procedures). improving maladaptive social cognition [40]. Thus, it seems worth considering provision of training on basic social percep- Experiment 4. Anxiety and Loneliness tion skills such as detecting eye gaze direction as an interven- Sixty-one participants (aged 18–39, mean 23.5 6 SD 4.5, 43 females) from tion to reduce loneliness. Conversely, it is also possible that the population studied in experiment 1 completed the STAI for trait anxiety consisting of 20 question items (Form Y) [46]. socially isolated individuals have less frequent social contacts and therefore have less opportunity to develop sensitivity to Experiment 5. Empathy and Loneliness social visual cues. This hypothesis predicts that social envi- Ninety-five participants (aged 18–39, mean 22.3 6 SD 4.3, 53 females) ronment changes (e.g., freshmen who leave family and friends from the population studied in experiment 1 completed the Interpersonal behind or people who start living alone) that make people Reactivity Index (IRI) questionnaire consisting of 28 question items [24]. lonely [41] would impact on basic social perception skills. There were four subscales: fantasy scale (FS), perspective taking (PT), Longitudinal or intervention studies will be particularly useful personal distress (PD), and empathic concern (EC) (see [24] for full details of the questionnaire). to disentangle complex relationships between loneliness, social perception skills, and relevant brain areas. Supplemental Information Experimental Procedures Supplemental Information includes two figures, one table, two experiments, and Supplemental Experimental Procedures and can be found with this Experiment 1. Voxel-Based Morphometry of Loneliness article online at http://dx.doi.org/10.1016/j.cub.2012.08.045. Participants A total of 108 healthy volunteers with normal or corrected to normal vision Acknowledgments (aged 18–32, mean 23.5 6 4.37 SD, 62 female) were recruited from the University College London subject pool. The experiments were approved This work was supported by the Wellcome Trust (G.R.), Japan Society for by the local ethics committee, and participants gave written informed the Promotion of Science and Japan Science and Technology Agency consent. (R.K.), British Academy postdoctoral fellowship (B.B.; M.J.B.), the Danish Assessment of Loneliness National Research Foundation and the Danish Research Council for Culture All participants were asked to fill out the UCLA Loneliness Scale Question- and Communication (B.B.), the European Union MindBridge project (B.B.), naire [8]. and ESRC (B.D.; M.J.B.). The Wellcome Trust Centre for Neuroimaging is MRI Data Acquisition and Analysis supported by core funding from the Wellcome Trust 091593/Z/10/Z/. MR images were acquired on a 1.5-T Siemens Sonata MRI scanner (Siemens Medical, Erlangen, Germany) using a T1- weighted 3D Modified Received: January 13, 2012 Driven Equilibrium Fourier Transform (MDEFT) sequence. 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Brain Structure Links Loneliness to Social Perception

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Current Biology 22, 1975–1979, October 23, 2012 ª2012 Elsevier Ltd. Open access under CC BY license. http://dx.doi.org/10.1016/j.cub.2012.08.045 Report Brain Structure Links Loneliness to Social Perception 1, 1,2,3 4 Ryota Kanai, * Bahador Bahrami, Brad Duchaine, the pSTS cluster (Figure 1). The peak voxel was situated within 5 1,5 1,2 Agnieszka Janik, Michael J. Banissy, and Geraint Rees the middle temporal gyrus (T[103] = 4.66, Z = 4.42, R = 0.174, UCL Institute of Cognitive Neuroscience, 17 Queen Square, p[FWE-corr] = 0.02, MNI coordinate x = 248, y = 269, z = 15). London WC1N 3AR, UK We did not find any significant cluster that positively correlated Wellcome Trust Centre for Neuroimaging, Institute of with loneliness (p[corr] > 0.05 nonstationary correction; see Neurology, University College London, 12 Queen Square, Table S1 available online for uncorrected results). London WC1N 3BG, UK Given the known functions of pSTS in social perception Interacting Minds Project, Institute of Anthropology, [16, 17], it appears unlikely that the volume of the left pSTS Archaeology, Linguistics, Aarhus University, and Centre of directly mediates subjective experiences of loneliness per Functionally Integrative Neuroscience, Aarhus University se. The pSTS region is thought to be involved in initial stages Hospital, Norrebrogade 44, Building 10 G, of social perception combining different sensory cues such 8000 Aarhus C, Denmark as eye gaze, hand action, and body movements [16]. In partic- Department of Psychological and Brain Sciences, Dartmouth ular, the position of the pSTS cluster revealed in our VBM result College, Moore Hall 6207, Hanover, NH 03755, USA is close to the locus where activations are elicited when Department of Psychology, Goldsmiths, University of viewing the eye gaze of others [18]. Specifically, our pSTS London, New Cross, London SE14 6NW, UK locus overlapped with the mean coordinate of the loci sensi- tive to eyes (x = 248, y = 255, z = 6; see [16] for a meta- analysis). Summary Experiment 2. Social Perception and Loneliness Loneliness is the distressing feeling associated with the Taking our findings from experiment 1 with the previously perceived absence of satisfying social relationships [1]. established functional role of pSTS leads to the intriguing Loneliness is increasingly prevalent in modern societies hypothesis that lonely individuals might have deficits in basic [2, 3] and has detrimental effects on health and happiness social perception. [4, 5]. Although situational threats to social relationships We tested this hypothesis in a subset of the original partici- can transiently induce the emotion of loneliness, suscepti- pants (n = 22) using a gaze perception task. Participants were bility to loneliness is a stable trait that varies across individ- shown three faces and asked to judge which face showed uals [6–8] and is to some extent heritable [9–11]. However, strabismic gaze (eyes not aligned properly). We found that little is known about the neural processes associated with the ability to process eye gaze information was negatively loneliness (but see [12–14]). Here, we hypothesized that correlated with self-reported loneliness (Figure 2A; R = 20.51, individual differences in loneliness might be reflected in T[20] = 22.64, p = 0.015). We replicated this association in an the structure of the brain regions associated with social independent sample (n = 38) using a more naturalistic gaze processes [15]. To test this hypothesis, we used voxel-based task and confirmed the specificity of this association, because morphometry and showed that lonely individuals have less it was not observed for a nonsocial face perception task (see gray matter in the left posterior superior temporal sulcus Experiment S1 and Figure S1). Moreover, the efficiency of (pSTS)—an area implicated in basic social perception. As eye gaze processing was significantly correlated with the this finding predicted, we further confirmed that loneliness regional gray matter volume of the pSTS cluster (Figure 3A; was associated with difficulty in processing social cues. R = 0.441, T[20] = 2.21, p = 0.038). Although other sociopsychological factors such as social Although the results so far suggest that pSTS, eye gaze pro- network size, anxiety, and empathy independently contrib- cessing, and loneliness are linked with one another, whether uted to loneliness, only basic social perception skills the gaze perception ability mediates the relationship between mediated the association between the pSTS volume and the volume of pSTS and loneliness remained uncertain. We loneliness. Taken together, our results suggest that basic therefore computed the partial correlation between pSTS social perceptual abilities play an important role in shaping volume and loneliness while regressing out the contribution an individual’s loneliness. of eye gaze performance. This revealed that the original sig- nificant correlation between pSTS gray matter volume and loneliness in this sample (R = 20.454, p = 0.03) vanished after Results controlling for individual differences in eye gaze performance (R = 20.138, p = 0.550). This supports the notion that the Experiment 1. Voxel-Based Morphometry of Loneliness negative correlation between pSTS volume and loneliness We correlated brain structure and reported loneliness in a was mediated by the efficiency of perceiving eye gaze. sample of 108 healthy adults (see Experimental Procedures) To examine whether the relationship between loneliness and and found a large significant cluster in the posterior superior social perception via pSTS was specific to eye gaze per- temporal sulcus (pSTS) in which the regional gray matter ception, we examined participants’ abilities on several other volume negatively correlated with individual differences in types of social perception tasks, namely, facial expression loneliness (cluster size = 3,837 mm , p[corr] < 0.05 nonsta- discrimination [19, 20], facial identity discrimination [19, 20], tionary). Lonely individuals had smaller gray matter volume in and facial emotion recognition [20, 21]. The correlation between loneliness and the ability to discriminate facial *Correspondence: [email protected] emotional expressions did not reach statistical significance Current Biology Vol 22 No 20 of the original participants (n = 45). We found that although social network size was strongly correlated with the loneliness scale (R = 20.617, T[43] = 25.144,p < 0.001), factoring out the social network scale did not affect the pSTS-loneliness corre- lation (R = 20.395, T[42] = 22.789, p = 0.008; original correla- tion in this sample, R = 20.386, T[42] = 22.743, p = 0.009). There was also no correlation between pSTS size and the social network scale (R = 0.125, T[43] = 20.823, p = 0.413), because the overlap between the pSTS cluster for loneliness the cluster previously reported for online social network size overlapped only less than 1% (see Figure S2). These results together indicate that the left pSTS gray matter volume and social network size independently predict an individual’s loneliness. Experiment 4. Trait Anxiety and Loneliness Loneliness scores are correlated with other mood factors such as anxiety and depressive symptoms [23]. To examine whether such mood measures mediated the association between the volume of pSTS and loneliness, we administered the STAI inventory to collect data on trait anxiety from 61 of our original participants in experiment 1. We replicated previous findings [23] showing that trait anxiety is highly correlated with loneliness score (R = 0.596, p < 0.001). We extracted the pSTS volume from MRI scans of this subpopulation of participants and found that trait anxiety also showed a tendency to negatively correlate with Figure 1. Gray Matter Volume Correlated with Loneliness Scale pSTS volume, but this did not reach statistical significance (A) The left STS in which variability in gray matter volume exhibited signifi- (R = 20.226, p = 0.08). Because this subpopulation was cant negative correlation with loneliness scale (n = 108) is superimposed selected from the participants in experiment 1, we observed on a standard T1-weighted template brain in MNI stereotactic space. The the expected negative correlation between loneliness score significant cluster is shown at t > 2.3 for visualization purpose. (B) A scatterplot between loneliness scale and pSTS volume adjusted for and pSTS volume in this subsample (R = 20.596, p < 0.001). age, gender, and total gray matter volume is shown for illustration purpose To examine whether this correlation was (partially) mediated only. Statistical inference was based on the p value corrected for multiple by trait anxiety, we tested whether the correlation was weak- comparisons across the whole brain at a cluster level with nonstationary ened by inclusion of anxiety as a covariate. However, the lone- correction [44]. liness-pSTS correlation was unaffected by regressing out the contribution of anxiety (R = 20.568, p < 0.001). These results (Figure 2B; R = 20.376, T[20] = 21.81, p = 0.085). However, indicate that the volume of left pSTS and trait anxiety indepen- this performance was significantly correlated with the gray dently contribute to loneliness score. matter volume in the pSTS cluster (Figure 3B; R = 0.492, T[20] = 2.528, p = 0.020). Similarly, sensitivity to face identity Experiment 5. Empathy and Loneliness did not correlate with loneliness (Figure 2C; R = 20.167, Finally, we examined whether loneliness was associated with T[20] = 20.759, p = 0.457) but significantly correlated with aspects of empathy using the Interpersonal Reactivity Index the gray matter volume in the pSTS cluster (Figure 3C; R = (IRI), which measures fantasy scale (FS), perspective taking 0.544, T[20] = 2.899, p = 0.009). Performance in the emotion (PT), personal distress (PD), and empathic concern (EC) recognition task (measured by efficiency score) did not signif- [24, 25]. We collected these IRI subscales from a subset (n = icantly correlate with loneliness (Figure 2D; R = 0.258, T[20] = 95) of the participants studied in experiment 1. We found 1.19, p = 0.257) or the gray matter volume in the pSTS cluster that the loneliness score significantly correlated with PD (Figure 3D; R = 0.403, T[20] = 1.97, p = 0.063). Taken together, (T[93] = 3.59, R = 0.349, p < 0.01, Bonferroni corrected), but loneliness was correlated with the perception of eye gaze, not with other subscales (FS, T[93] < 1, R = 0.028, p = 0.316; whereas the gray matter volume of the left pSTS correlated PT, T[93] = 21.97, R = 20.200, p = 0.208; EC, T[93] = 22.30, more broadly with processing social cues from faces. R= 20.233, p = 0.092, Bonferroni corrected). This is in line with previous reports that people with a high PD score show Experiment 3. Social Network Size and Loneliness poor social perception and social competence [24] and further Next, we examined whether social network size could explain supports our findings that loneliness is related to reductions in the correlation between loneliness and pSTS. Previously, we social perception. None of these subscales were, however, have shown that the gray matter volume of the middle significantly associated with the volume of the left pSTS (all temporal gyrus (MTG) region abutting the pSTS region associ- p > 0.05). ated with loneliness correlates with online social network size [22]. Thus, it is possible that the link between pSTS and Discussion loneliness was mediated by individual differences in social network size. We therefore examined whether the pSTS- Our experiments show that individual differences in the loneliness correlation could be explained by social network expressed trait of loneliness are linked with variations in size by collecting data on social network size from a subset the gray matter volume of left pSTS. This region has been Loneliness and Social Perception Figure 2. Relationship between Loneliness Scale and Performances for Social Perception Tasks (n = 22) Abnormal gaze detection task (A), same-different emotion discrimination task (B), same-different identity discrimination task (C), and films emotion recognition task (D). See Experimental Proce- dures for full details of the tasks. Specifically, lonely individuals show weaker activation in the ventral striatum when viewing pictures of pleasant social events than when viewing pleasant pictures of nonsocial objects, whereas this pattern is reversed for nonlonely individuals. Furthermore, lonely individ- uals show weaker activations in bilateral temporoparietal junction (TPJ) to unpleasant social pictures of people compared to unpleasant pictures of objects. Although functional and struc- tural correlates of loneliness may be regionally dissociated, both the previous functional study [14] and our current study point to the idea that loneliness is reflected in the way the brain processes visually presented social cues. In future research, conjoint measurements of structure and function will be needed to establish their relationships. implicated in several fundamental aspects of processing The correlation we observed between pSTS and loneliness social information. However, it is unlikely that pSTS directly seems to be specifically mediated by the ability to process (or any other single brain area per se) mediates such a complex eye gaze information, because factoring out the eye gaze performance abolished the correlation between pSTS and cognitive quality as the transient feeling of loneliness. This brain region is causally involved in perception of social stimuli loneliness. This was not observed with other measures such such as biological motion [26, 27] and gaze direction [28], sug- as social network size, anxiety, and empathy (personal gesting that the feeling of loneliness may be associated with distress in particular) that were correlated with loneliness. deficits in these basic social perceptual skills. Our behavioral These results suggest that a multitude of social and psycho- experiments confirmed this hypothesis by showing significant logical factors contribute to loneliness score, but their correlations between individual variability on the reported association with loneliness is independent of the pSTS struc- loneliness scale and objectively measured skills relevant to ture. We speculate that interindividual differences in those social perception such as the performance of eye gaze factors may also have a basis in the structure of other brain perception. Furthermore, the volume of pSTS also predicted regions [22, 25, 36–39], but their associations with loneliness such basic social skills, which confirms the relevance of the may have been too weak to be detected within our current same pSTS region in those social perception tasks. sample size (n = 108). Further investigation with a larger Our findings indicate that lonely individuals have deficits at sample may help reveal more regions that are relevant for individual differences in loneliness. Future studies may benefit a relatively early stage of processing social cues. Lonely indi- viduals are low in social skills [29, 30] and have poor sensitivity from asking participants under what kind of circumstances to nonverbal communication [31], whereas they are proficient they feel lonely, because such qualitative data may help us in verbal communication [32]. People with poor social skills are understand how multiple pathways lead to loneliness in more likely to become lonely when they encounter negative different individuals. stressful life events [33]. This finding is in line with the hypoth- Because of the cross-sectional nature of our present study, esis that social skills deficits are antecedents of loneliness we cannot determine the direction of causation between lone- [34]. However, it should be noted that in those studies, social liness, social perceptual abilities, and the volume of the left skills were measured by different methods such as question- pSTS. One appealing possibility is that poor ability to recog- naires (e.g., the Social Skills Inventory, [35]) and it remains nize social cues may lead to social isolation and loneliness. unclear whether social skills measured by questionnaire items For example, people who are poor at reading social cues (e.g., ‘‘At parties I can instantly tell when someone is interested may experience difficulty in developing social relationships. in me.’’) correspond to basic aspects of social perception This hypothesis predicts that improvements in social percep- measured in the laboratory as here. tion by training may increase the quality and quantity of social Subjective loneliness modulates brain activations to interaction and thereby mitigate the degree of subjective lone- pleasant and unpleasant pictures of other people [14]. liness. A recent meta-analysis of intervention studies that Current Biology Vol 22 No 20 Figure 3. Relationship between Regional pSTS Volume and Behavioral Performances in Social Perception Tasks (n = 22) Abnormal gaze detection task (A), same-different emotion discrimination task (B), same-different identity discrimination task (C), and films emotion recognition task (D). See Experimental Proce- dures for full details of the tasks. and total gray matter volume of individual brains were included in the design matrix as covariates of no interest. We used a threshold of p(corr) < 0.05 corrected for multiple compari- sons at a cluster level using nonstationary correction [44]. Experiment 2. Social Perception and Loneliness We contacted the participants in experiment 1 and asked them to take part in follow-up experi- ments. A total of 22 healthy volunteers (aged 19–30, mean 22.7 6 SD 3.9, 15 females) were tested on four social perception tasks: abnormal gaze detection task, emotional expression dis- crimination task, identity discrimination task, and films emotion recognition task (see Supple- mental Experimental Procedures for full details). Experiment 3. Social Network Size and Loneliness Forty-five participants recruited from the UCL student community (aged 18–30 mean 23.2 6 SD 3.6, 52 females) completed the social network size questionnaire [45]. A normalized aimed to reduce loneliness with various strategies showed social network size was computed for each participant by averaging the Z scores for all the questions items (see Supplemental Experimental that the most effective intervention for treating loneliness is Procedures). improving maladaptive social cognition [40]. Thus, it seems worth considering provision of training on basic social percep- Experiment 4. Anxiety and Loneliness tion skills such as detecting eye gaze direction as an interven- Sixty-one participants (aged 18–39, mean 23.5 6 SD 4.5, 43 females) from tion to reduce loneliness. Conversely, it is also possible that the population studied in experiment 1 completed the STAI for trait anxiety consisting of 20 question items (Form Y) [46]. socially isolated individuals have less frequent social contacts and therefore have less opportunity to develop sensitivity to Experiment 5. Empathy and Loneliness social visual cues. This hypothesis predicts that social envi- Ninety-five participants (aged 18–39, mean 22.3 6 SD 4.3, 53 females) ronment changes (e.g., freshmen who leave family and friends from the population studied in experiment 1 completed the Interpersonal behind or people who start living alone) that make people Reactivity Index (IRI) questionnaire consisting of 28 question items [24]. lonely [41] would impact on basic social perception skills. There were four subscales: fantasy scale (FS), perspective taking (PT), Longitudinal or intervention studies will be particularly useful personal distress (PD), and empathic concern (EC) (see [24] for full details of the questionnaire). to disentangle complex relationships between loneliness, social perception skills, and relevant brain areas. Supplemental Information Experimental Procedures Supplemental Information includes two figures, one table, two experiments, and Supplemental Experimental Procedures and can be found with this Experiment 1. Voxel-Based Morphometry of Loneliness article online at http://dx.doi.org/10.1016/j.cub.2012.08.045. Participants A total of 108 healthy volunteers with normal or corrected to normal vision Acknowledgments (aged 18–32, mean 23.5 6 4.37 SD, 62 female) were recruited from the University College London subject pool. The experiments were approved This work was supported by the Wellcome Trust (G.R.), Japan Society for by the local ethics committee, and participants gave written informed the Promotion of Science and Japan Science and Technology Agency consent. (R.K.), British Academy postdoctoral fellowship (B.B.; M.J.B.), the Danish Assessment of Loneliness National Research Foundation and the Danish Research Council for Culture All participants were asked to fill out the UCLA Loneliness Scale Question- and Communication (B.B.), the European Union MindBridge project (B.B.), naire [8]. and ESRC (B.D.; M.J.B.). The Wellcome Trust Centre for Neuroimaging is MRI Data Acquisition and Analysis supported by core funding from the Wellcome Trust 091593/Z/10/Z/. MR images were acquired on a 1.5-T Siemens Sonata MRI scanner (Siemens Medical, Erlangen, Germany) using a T1- weighted 3D Modified Received: January 13, 2012 Driven Equilibrium Fourier Transform (MDEFT) sequence. 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Published: Oct 1, 2012

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