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. 2012 Sep;14(3):319–351. doi: 10.31887/DCNS.2012.14.3/gdichter

Table I. Studies investigating face processing in autism spectrum disorders. ASD: Autism Spectrum Disorder; TYP: Neurotypical; †ASD refers to the entire autism sample in a particular study, including high functioning autism, Asperger's syndrome, and pervasive developmental disorder not otherwise specified; *Total number of participants is presented first followed by the number of females in parentheses, if reported; **Not specified; ↓: decreased activation; ↑: increased activation. Abbreviations used in tables: ACC, anterior cingulate cortex; ACG, anterior cingulate gyms; AG, angular gyms; Al, anterior insula; AMY, amygdala; ATL, anterior temporal lobe; BA, Broca's area; BG, basal ganglia; CM, caudate nucleus; DAC, dorsal anterior cingulate; DLPFC, dorsolateral prefrontal cortex; DMPFC, dorsomedial prefrontal cortex; DN, dentate nucleus; FFA, fusiform face area; FG, fusiform gyms; IC, insular cortex; IFA, inferior frontal area; IFC, inferior frontal cortex; IFG, inferior frontal gyrus; IPL, inferior parietal lobe; ITG, inferior temporal gyrus; LG: lingual gyrus; LSTG, left superior temporal gyrus; MCG, >middle cingulate gyrus; MFC, midfrontaI cortex; MFG, midfrontal gryus; MFL, medial frontal lobes; NAC, nucleus accumbens; OFC, orbitofrental cortex; OFG, orbitofrental gyrus; MPFC, medial prefrontal cortex; MTG, medial temporal gyrus; PO, pars opercularis; PCC, posterior cingulate cortex; PFC, prefrontal cortex; PHG, parahippocampal gyrus; PL, parietal lobe; PMC, premotor cortex; PVC, primary visual cortex; RPVC, right primary visual cortex; SFG, superior frontal gyrus; SPL, superior parietal lobe; STG, superior temporal gyrus; STS, superior temporal sulcus; THAL, thalamus; TL, temporal lobe; TPJ, temporoparietal junction; VS, ventral striatium; VLPFC, ventrolateral prefrontal cortex; VOC, ventral occipital cortex; VMPFC, ventromedial prefrontal cortex; WA, Wernicke's Area .

Citation ASD*† TYP*† ASD age TYP age Task(s) Core findings in ASD group (relative to controls) Conclusions
Ashwin, Baron-Cohen, Wheelwright, O'Riordan, Bullmore, 2007 [163] 13 (13) 13 (13) 31.2 + 9.1 25.6 + 5.1 Viewed facial stimuli known to activate AMY in healthy controls Differential activation to faces; ↑ACG, superior temporal cortex; No difference in AMY activation between angry and frightened faces Different activation of social brain during face processing; Absence of response to varying emotional intensity of facial stimuli
Bird, Catmur, Silani, Frith, Frith, 2006 [164] 16 (14) 16 (14) 33.3 ± 11.5 35.3 + 12.1 Viewed pairs of stimuli (face/ house) in attended /unattended locations Attention modulation present only to house images (rather than to both houses and faces) Social stimuli less salient for individuals with ASD
Bookheimer, Wang, Scott, Sigman, Dapretto, 2008 [165] 12 (12) 12 (12) 11.3 ± 40 11.9 ± 2.4 Inverted or upright face matching ↓Frontal cortex across all conditions, particularly left hemisphere, dorsal IFG (i.e. mirror neurons); ↓AMY; ↑Precuneus Faces processed as objects; Behavioral differences in processing upright vs inverted faces implicates a social rather that visual processing impairment
Corbett, Carmean, Ravizza, et al, 2009 [166] 12 (12) 15 (13) 9.01 ± 13.82 9.17 ± 1.44 Face identify and expression matching ↓AMY during expression matching; ↓FG during identity matching ASD recruits frontal and parietal lobes, but not AMY, for face expression matching; ASD processes faces less efficiently and less effectively; AMY fails to provide socio-emotional context during social interactions
Coutanche, Thompson-Schill, Schultz, 2011 [167] 12 (12) 12 (12) 13.9 ± 4.48 13.6 ± 3.87 Recognition of emotional facial expressions Multi-voxel pattern analysis classification negatively correlated with symptom severity (activation levels did not); Searchlight analysis across the ventral TL identified regions with relationships between classification performance and symptom severity Clinical severity was more classifiable from MVPA than from FG patterns; MVPA can identify regions not found using mean activation, ITG may play a role in ASD face processing
Dalton, Nacewicz, Johnstoner, et al, 2005 [168] Task : 14 (14) Task 2 : 16 (16) Task 1: 12 (12) Task 2: 16 (16) 15.9 ± 4.71 17.1 ± 2.78 (1) Facial emotion discrimination (2) Face recognition ↓Bilateral FG, occipital gyri, MFG; ↑Left AMY, OFG; FG and AMY activation correlated with time fixating on eye regions in the ASD group Diminished gaze fixation may account for FFG hypoactivation results in the literature
Deeley, Daly, Surguladze, et al, 2007 [169] 18 (18) 9 (9) 34 + 10 27 ± 5 Viewed face stimuli with variable emotional expressions Fusiform, extrastriate hyporesponsiveness across emotion and intensity levels While fusiform and extrastriate regions are activated to social stimuli in ASD, it is less so than in typical development
Greimel, Schulte-Ruther, Kircher, et al, 2010 [170] 15 (15), 11 (11) (adolescents, fathers) 15 (15), 9 (9) (adolescents, fathers) 14.9 ± 1.6, 47.7 ± 5.3 (adolescents, fathers) 15.0 ± 1.4, 43.9 ± 5.1 (adolescents, fathers) Emotion identification in facial stimuli and in self ↓FG correlated with social deficits, ↓IFG during self-task; Fathers of ASD performed similarly to fathers of controls, but showed ↓FG FG impairment shared between first-degree relatives is a fundamental feature of ASD; FG impairment during face processing related to empathy deficits
Hadjikhani, Joseph, Snyder, et al, 2004 [171] 11** 10** 36 ± 12 26 ± 6 Viewed faces, objects, and scrambled images No FFA activation differences when viewing faces Face processing abnormalities not due to dysfunction in the FFA, but to abnormalities in surrounding networks involved in social cognition
Hadjikhani, Joseph, Snyder, Tager-Husberg, 2007 [172] 10** 7** 34 ± 11 35 ± 12 Viewed unemotional faces No differences in FFA, inferior occipital gyrus activation; ↓Right AMY, IFC, STS, somatosensory cortex, PMC Atypical activation in a broader face-processing network outside of FFA and inferior occipital gyrus; Suggests mirror neuron system disturbance during face-processing in ASD
Hall, Szeehtman, Nahmias, 2003 [173] 8 (8) 8 (8) ** ** Emotion and gender recognition tasks ↓IFA, FG; ↑right ATL, ACG, THAL Recognition of emotions in ASD achieved through recruitment of brain regions concerned with attention, perceptual knowledge, and categorization
Hall, Doyle, Goldberg, West, Szatman, 2010 [174] 12 (12) 12(12) 31.8** 32** Identified gender of subliminally presented images of anxious faces ↓FFA; No AMY differences between groups Transmission of social information along subcortical pathways intact, but signaling to downstream structures as well as the mechanisms of subsequent processing are impaired
Hubl, Bolte, Feineis-Matthews, et al, 2003 [175] 10 (10) 10 (10) 25.3 ± 6.9 27.7 ± 7.8 Viewed faces and complex patterns ↓FG, esp during face processing; ↑Medial occipital gyrus, superior parietal lobule, medial frontal gyrus Deficits in face-specific regions, but overdevelopment in areas of visual search; Predisposed for local processing, rather than global
Humphreys, Hasson, Avidan, Minshew, Behrmann, 2008 [176] 13 (13) 15 (15) 27 ± 10 29 ± 10 Viewed faces, buildings, objects and patterns in controlled and naturalistic settings ↓FFA, occipital face area, STS in response to faces; No group differences in place-related or object-related processing Differential organization of ventral visual cortex; Developmental effects of lower functional connectivity have a more pronounced effect on later-developing systems, like face-processing, than for early-developing systems, like object- and place-processing
Kleinhans, Richards, Sterling, et al,2008 [177] 19** 21** 23.5 ± 7.8 25.1 ±7.6 Viewed familiar faces, houses Reduced functional connectivity FFA-AMY, FFA-PCC, FFA-THAL; Greater social impairment correlated with worse connectivity FFA-AMY, FFA-right IFC Abnormal connectivity in limbic system underlies social deficits in ASD
Kleinhans, Johnson, Richards, et al, 2009 [178] 19** 20** ** ** Viewed neutral faces Reduced bilateral AMY habituation;No group differences in FG habituation AMY hyperarousal to socially relevant stimuli; Sustained AMY arousal may contribute to social deficits
Kleinhans, Richards, Weaver, et al, 2010 [179] 31 (29) 25 (23) 23.57 ± 6.6 23.32 ± 5.15 Matched facial expressions of fear or anger ↓Left PFC; ↑Occiptal lobe; Social anxiety correlated with ↑right AMY, ↓left middle temporal gyrus, ↓FFA Social anxiety mediates emotional face perception
Kleinhans, Richards, Johnson, et al, 2011 [180] 31 (29) 25 (23) 23.57 ± 6.6 23.32 ± 5.15 Viewed images of faces and houses No activation in right AMY, right pulvinar, or bilateral superior colliculi to faces; Rapid face identification but failure to engage subcortical brain regions involved in face detection and automatic emotional face processing.
Koshino, Kana, Keller, et al, 2008 [181] 11 (11) 11 (10) 24.5 ± 10.2 28.7 ± 10.9 Working memory tasks using faces ↓Inferior left PFC, right posterior temporal; Activation in a different FFA location; Lower FFA-frontal connectivity Faces processed as objects; Working memory of faces not mediated by typical frontal regions
Loveland, Steinberg, Pearson, Mansour, Reddoch, 2008 [182] 5 (4) 4 (3) 18 ± 1.3 17 + 1.1 Auditory and visual emotional congruence task During emotion trials, ↓OFt, STG, PHG, posterior cingulate gyrus, occipital gyrus Fronto-limbic and superior temporal activity differences during integration of auditory and visual emotional stimuli
Monk, Weng, Wiggins, et al, 2010 [183] 12** 12** 26 ± 6 27 ± 6 Probe detection with different emotional expressions ↑Right AMY to emotional faces; Greater right AMY and VMPFC coupling; Weaker positive right AMY and TL coupling Attention must be factored into any model of neural circuitry in ASD; Overconnectivity may underlie greater emotional responses in ASD
Morita, Kosaka, Saito, et al, 2011 [184] 15 (14) 15 (13) 23.7 ± 4.3 23.3 + 3.6 Rated photogenicity of faces ↓Setf-related activity in PCC; ↓Right IC and lateral OFC to embarrassment; ↓IC activity to self-face images associated with weak coupling between cognitive evaluation and emotional responses to self-face Decoupling between evaluation of self-face images and emotional response; Dysfunction in PCC and IC contributes to lack of self-conscious behaviors in response to self-reflection
Ogai, Matsumoto, Suzuki, et al, 2003 [185] 5** 9** 21.8 ± 5.9 23.0 ± 5.2 Facial expression recognition ↓Left insula, left IFG, left putamen during recognition of disgust and fear Difficulty understanding facial expressions in others and, therefore, in manipulating social information
Pelphrey, Morris, McCarthy, Labar, 2007 [186] 8 (6) 8 (6) 24.5 ± 11.5 24.1 ± 5.6 Dynamic and static face processing ↓AMY, STS, FG to dynamic faces Dysfunctions in these component areas may contribute to problems in social and emotional processing
Perlman, Hudac, Pegors, Minshew, Pelphrey, 2011 [187] 12 (11) 7 (7) 25.5 ± 7.47 28.57 ± 5.74 Viewed faces while compelled to look at eyes Right FG activity normalized by following predetermined scan paths to eyes, but AMY response unaffected Rather than an underdeveloped FFA as a result of not focusing on faces during development, FFA appears functional; Impaired mechanism of appropriately directing gaze
Pierce, Muller, Ambrose, Allen, Courchesne, 2001 [188] 6 (6) 8 (8) 29.5 ± 8 28.3** Face perception with gender identification ↓Bilateral FG, left AMY; 50% of group showed atypical FG activation to faces ASD is associated with aberrant locations of maximal activations to faces
Pierce, Haist, Sedaghat, Courchesne, 2004 [189] 7 (7) 9 (9) 27.1 ± 9.2 ** Familiar versus unfamiliar face processing No group difference in extent of FFA activation to faces; ↑FFA to familiar faces. Right hemisphere dominance to both types of faces; Limited response in the posterior cingulate, AMY, MFL FFA hypoactivation to faces in ASD may be specific to unfamiliar faces; ASD may be characterized by anomalous FFA modulation by faces, rather than hypoactivation
Pierce, Redcay, 2008 [190] 11 (9) 11 (9) 9.9 ± 2.1 9.8 ± 1.8 Matched faces of mothers, other children, adult strangers Normal FG response to face of mother or other children; ↓FG to stranger adult faces Selective reduction in FG activity in response to strangers may be a result to reduced attention and interest in those conditions
Pinkham, Hopfinger, Peiphrey, Pwen, Penn, 2008 [191] 12** 12** 24.08 ± 5.71 27.08 ± 3.99 Free-viewing face processing ↓Right AMY, FFA; ↓Left VLPFC compared to non-paranoid individuals with schizophrenia Potential common substrates of impaired social cognition in ASD and schizophrenia
Rudie, Shehzad, Hernandez, et al, 2011 [192] 23 (21) 25 (22) 12.6 ± 2.83 13.3 ± 96 Emotional face processing Reduced functional integration; AMY-secondary visual areas, PO-parietal cortex, Reduced segregation AMY-DLPFC, PO-VMPFC; Reduced integration PO-FC, within right NAC Reduced functional integration and segregation of large-scale brain networks during face viewing
Scherf, Luna, Minshew, Behrmann, 2010 [193] 10 (10) 10 (10) 12.2 ± 1.1 11.2 ± 1.3 Vignettes of faces, common objects, houses and scenes of navigation ↓FG occipital face area, STS to faces; ↑Ventral posterior FG to faces Selective ventral visual pathway disruption; Face-processing alteration present in early adolescence, Face perception in ASD akin to object perception in typical development
Schultz, Gauthier, Klin, et aI, 2000 [194] 14 (14) 28 (28) (2 groups of 14) 24.08 ± 5.71 27.08 ± 3.99 Face discrimination ↓Right FG; ↑Right ITG Brain activation in the ASD group during face discrimination was consistent with feature-based strategies
Uddin, Davies, Scott, et al, 2008 [195] 18 (18) 12 (12) 13.19 ± 2.61 12.23+2.10 Judged “self” or “other” for morphed face images ↓Right premotor/prefrontal during presentation of “other” faces Functional dissociation between the representation of self versus others suggests a neural substrate of self-focus and decreased social understanding
Wang, Dapretto, Hariri, Sigman, Bookheimer, 2004 [196] 12 (12) 12 (12) 13.91 ± 2.61 12.23 ± 2.10 Emotion matching naming ↓FG and ↑precuneus during matching facial expressions; Lack of modulation by task demands in the AMY Recruited different neural networks and relied on different strategies when processing facial emotion
Welchew, Ashwm, Berkouk, et al, 2005 [197] 13 (13) 13 (13) 31.2 ± 51 25.6± 5.1 Face processing Abnormal AMY—parahippocampal connectivity Difficulty in grasping facial expressions in others and, therefore, in manipulating interpersonally derived information
Weng, Carrasco, Swartz, et al, 2011 [198] 22 (17) 20 (19) 14.36 ± 17 14.97 ± 1.95 Emotional face processing ↑AMY, ventral PFC and striatum, particularly to sad faces; Negative correlation between age, pubertal status, and AMY activation Greater activation in social-emotional processing regions when viewing faces