We found that individuals with high-functioning autism or Asperger’s syndrome give similar average subjective ratings of the roughness and pleasantness of textured surfaces to their typical peers, although with more variability, particularly for the neutral burlap stimulus, and a slight tendency to find the least pleasant (mesh) stimulus rougher and less pleasant than did the control group (see ). We also noted that, consistent with prior work [Guest et al., 2009
], there is a negative relationship between perceived roughness and perceived pleasantness for these textures in both groups.
The increased variability in responses of the ASD group is consistent with a variety of studies demonstrating the profound heterogeneity of the disorder [for a review, see, Happe, Ronald, & Plomin, 2006
]. From clinical phenotype to neural signatures [Müller, Kleinhans, Kemmotsu, Pierce, & Courchesne, 2003
; Toal et al., 2010
], heterogeneity in ASD is a pervasive challenge to autism research, prompting a growing emphasis on alternatives to case-control design [Towgood, Meuwese, Gilbert, Turner, & Burgess, 2009
]. However, it is interesting to note that the increased response variability in the ASD group was much higher than controls only for the neutral burlap texture, suggesting that ratings are less consistent for the ASD group when the perceptual attributes of a stimulus are more ambiguous. The idea that the ASD group is challenged by evaluating neutral or ambiguous stimuli is also supported by group differences in the correlations between perceived roughness and pleasantness. While this relation was consistently high and significant for both groups, it was significantly higher for ASD than control for the burlap texture. This suggests that for an affectively neutral stimulus, adults with ASD depend more heavily on the sensory aspects of the stimulus to determine their affective ratings than controls. This could be interpreted as an overly “literal” understanding of the relation between sensory and affective qualities of a more ambiguous stimulus by the ASD group.
We also noted session effects in the psychophysical portion of the study, generally consistent with recent work illustrating effects of prior exposure on affective ratings of touch [Löken, Evert, & Wessberg, 2011
]. The pattern of results we observed were that pleasant textures stay the same or improve slightly with repetition, while the perception of unpleasantness or roughness of the mesh texture tended to get worse with repeated exposure. suggests that the latter effect was especially true for the ASD group, while the former effect was weaker for ASD than controls. The phenomenon of stimulus satiation for pleasant stimuli is described in the gustatory system [Hetherington, Pirie, & Nabb, 2002
], and it is possible that a similar ceiling effect occurred across sessions with the brush stimulus. Likewise, anticipatory effects for the less pleasant stimuli after prior exposure may have resulted in lower pleasantness ratings for the other textures, particularly for the ASD group, for whom increased anxiety has been found to relate strongly anticipation, sensory stimuli, and unpleasant events [Gillott, & Standen, 2007
Although the group differences in the psychophysical responses to textures with a range of previously established roughness and pleasantness were subtle, we noted significant differences in the patterns of neural response in relevant areas of somatosensory and sensory integration cortex. While the control group showed significant increases in BOLD response to all three textures relative to rest, the ASD group showed a much less extensive pattern of response. The network activated in controls reflects primary and higher order somatosensory processing regions in the parietal lobe, such as the inferior parietal lobule, which is involved in somatosensory discrimination of objects [Reed et al., 2005
] and vibrotactile frequency [Soros et al., 2007
], and is heavily involved in multisensory integration [Mesulam et al., 1977
] that is critical for the development of social and communication skills [Macaluso et al., 2004
]. In addition, frontal areas such as the inferior frontal gyrus have been implicated in attention to tactile stimuli [Hagen et al., 2002
], haptic perception and multisensory integration of texture stimuli [Sathian et al., 2011
], as well as perception of socially relevant information such as facial expression [Bastiaansen et al., 2011] and general stimulus evaluation [Downar et al., 2002
The integration of somatic information with social perception in these regions may be important for the ability to map another’s body surface onto one’s own and to use this mapping to interpret the meaning of others’ actions, a significant deficit in ASD [Williams, 2008
]. Recently, the inferior frontal gyrus and inferior parietal lobule were both implicated in the visual and tactile perception of facial expressions [Kitada et al., 2010
], suggesting that these regions work together to support processing of socially relevant stimuli across sensory modalities. For the control group, the pattern of activation across these association areas was more extensive for pleasant and neutral textures than for the unpleasant mesh texture.
In contrast, the ASD group did not exhibit as widespread a pattern of activation beyond early somatosensory areas, and for the neutral texture did not exhibit any response at our a priori-determined threshold. Interestingly, while the control group had the most extensive activation for the pleasant brush texture, the ASD group’s most extensive pattern was for the unpleasant mesh texture; and in addition to contralateral SI and ipsilateral SII, included the inferior parietal lobule, suggesting increased attention to the unpleasant stimulation, and the insula, a region known for its role in evaluating somatosensory stimuli for their affective significance [Augustine, 1996
, Kulkarni et al., 2005
, McCabe et al., 2008
Group contrasts confirmed that the ASD response to all three textures was diminished compared to the control group. The control group had more signal increase than the ASD group in overlapping networks of regions including ipsilateral SI, bilateral MFG, and inferior parietal lobule for all three textures. The MFG has an established role in the experience [Prohovnik et al. 2004
] and perception of emotions [Sabatinelli et al., 2011
], and may have been involved in the affective response to the stimulation. The IFG is involved in maintaining and updating internal representations of bodily state and the skin’s surface [Spitoni, Galati, Antonucci, Haggard, & Pizzamiglio, 2010
; Wolpert, Goodbody, & Husain, 1998
]. Since these regions were less active in the ASD group for all three textures, it is likely that the neural representation of their affective valence and/or their effects on bodily state is atypical in ASD. For the more emotionally salient textures, brush and mesh, the cingulate cortex, a region involved in evaluating the affective significance of stimuli in preparation for action, was also more responsive in the control group. This finding in the anterior cingulate mirrors the results of Lindgren et al. 
who noted subgenual anterior cingulate activity in response to pleasant stroking touch.
For the most pleasant texture, the control group also exhibited a higher signal increase in the STG, a region that is important for assessing the social relevance of stimuli across sensory modalities [Pelphrey, Adolphs, & Morris, 2004
; Robins, Hunyadi, & Schultz, 2009
]. A recent study by Gordon et al. 
using similar gentle touch stimuli highlighted the superior temporal region as a multimodal node in the neural system for assessing social stimuli, including touch. This study also demonstrated responses in posterior insula and cingulate, findings with which our results are consistent. This suggests that the pleasant touch administered by the experimenter, an approximation of the gentle stroking touch that is characteristic of the CT afferent system, may have been differentially perceived as a socially relevant stimulus by the control group relative to the ASD group.
In group contrasts, the clusters in which the ASD response exceeded
that of controls were less numerous for all the three textures, and absent entirely for the burlap texture. For the unpleasant mesh texture, regions that were more active in ASD than control included right inferior parietal lobule as well as the insular cortex, suggesting increased neural resources devoted to attending to and evaluating the affective significance of these negative stimuli relative to the control group. This relative over-representation of unpleasant and under-representation of pleasant textures in the brain may constitute a neural mechanism for tactile defensiveness in ASD. The insula has reciprocal connections to multiple sensory and limbic regions (for a thorough review, see Nieuwenhuys, 2012
] and plays an important role in integrating internal and external cues to monitor the affective state of self and others [Decety & Chaminade, 2003
; Ruby & Decety, 2004
]. Further study of aberrant response in the insula may therefore shed light on its role within the neural networks that underlie complex social deficits that characterize ASD, such as empathy and emotion recognition.
These results suggest that individuals with ASD process affective touch stimuli differently than individuals without ASD. In general, they exhibit less response to stroked textures in classical somatosensory areas, including primary and secondary somatosensory cortex, as well as higher order somatosensory association areas located nearby the parietal and frontal regions. The neural representations that the ASD group did exhibit are most extensive for negative stimuli, and these unpleasant stimuli differentially recruited regions involved in evaluating emotional salience of somatosensory stimuli. Taken together, these data support the idea that the brain in people with ASD is hyporesponsive to pleasant tactile stimulation, and may be biased toward relative hyperresponsiveness to unpleasant tactile stimulation. It is possible that this imbalance gives rise to aberrant sensory responsiveness patterns that are linked with core symptoms of the disorder [Boyd et al., 2010
; Foss-Feig, Heacock, & Cascio, 2012
; Lane et al., 2010
; Watson et al., 2011
], although the specific association of sensory responsiveness patterns and core features is itself still under investigation. The observed differential neural signature based on stimulus type in the ASD group may also provide some clues about the behavioral copresentation of both hyper- and hyporesponsiveness to different stimuli within the same individual, a paradox that is prominent in phenomenological accounts of sensory responsiveness in ASD.
We found a preliminary support for this in the significant correlation between BOLD response in the insula during stimulation with the mesh and burlap textures and social and repetitive behavior deficits as measured by the ADI-R. It should be noted that the correlation coefficients were fairly modest, and P values were not corrected for multiple comparisons. This preliminary evidence, however, raises the possibility that aberrant neural responses to simple sensory stimuli are tied to the social and repetitive behavior abnormalities seen in ASD, the complexities of which are laid upon a much more basic foundation of affective response (rewarding or punishing) to sensory stimulation. Future studies should target the developmental course of affective responses to touch in the context of early social development in infants at risk for ASD.
Because our sample consisted of adults with ASD, we do not know the developmental time course of this aberrant neural signature in response to touch. An accurate representation of the bodily surface develops in the first few years of life [Brownell, Nichols, Svetlova, Zerwas, & Ramani, 2010
], and is important for social and cognitive abilities that necessitate differentiation of self from other [Schütz-Bosbach, Mancini, Aglioti, & Haggard, 2006
] and comparisons between self and other [Meltzoff, 2007
], which may be precursors to more complex social skills such as understanding others as intentional agents [Gallese, 2003
], and making inferences about others’ emotions, experiences, or intentions. These skills are among those impacted by the social deficits that define ASD. Further study of the impact of altered touch perception between the ages of two and three, when explicit topographic representation of the bodily surface emerges, [Brownell et al., 2010
] will provide important clues to how touch perception is linked to social behavior during development.
It was somewhat surprising to find such different neural response patterns in light of the similar perceptual reports of perceived pleasantness and roughness of the textures between the two groups. It is possible that the single stimulation in the psychophysical task was evaluated differently than the affective properties of the repeated stimulation in the scanner. It is also possible that the variability in the ASD pleasantness and roughness judgments obscured differences that might have been significant in a larger and/or less variable sample. Given the high IQ of our ASD sample and the straightforward nature of visual analog scale ratings, we do not attribute this discrepancy to impaired comprehension of the psychophysical task instructions. A limitation of our approach was the use of manual rather than automated brushing, which likely introduced variability in stimulation. Future work will replicate this study using an automated stimulator that will allow more complete control of speed and force of stimulation.