As predicted, thresholds on several psychophysical indices of tactile sensitivity were comparable between adults with autism and controls. Our finding that the von Frey tactile thresholds were unaltered compared with controls confirms the findings of O’Riordan and Passetti (2006)
, converging on the conclusion that the perceptual phenomenon of altered tactile sensitivity in autism as reported in the clinical literature, is not attributable to a difference in sensitivity to detecting light pressure against the skin as measured experimentally.
Our investigation of possible differences in neural adaptation to a suprathreshold vibrotactile stimulus also revealed no differences between our experimental group and controls. As is clear from , the autism group shows an adaptation-related elevation in threshold during the second block of trials, and then returns to the baseline threshold, as do controls. While it has long been demonstrated that peripheral afferents demonstrate fatigue in response to vibration exposure (Lundstrom & Johansson, 1986
), the adaptation tapped by this protocol is likely to reflect both peripheral and central neuronal activity (Bensmaia, Leung, Hsiao, & Johnson, 2005
; Goble & Hollins, 1993
; Whitsel et al., 2003
). Thus, failure of central neurons to adapt to somatosensory stimulation does not appear to account for reports of tactile hypersensitivity in autism.
For detection of the 33 Hz vibrotactile stimulus used in Experiment 2, we replicated the result of Blakemore et al. (2006)
at a similar frequency by demonstrating no group differences in thresholds on the palm at low frequencies of vibration. While we were encouraged by this consistency, it was not our explicit goal to replicate the entire Blakemore et al. study, thus we did not test the higher frequency vibration at which they noted group differences. However, at the forearm site, our group of adults with autism exhibited lower thresholds than the control group, indicating greater vibrotactile sensitivity, in spite of Experiment 1’s result that light touch sensitivity is similar in both groups regardless of testing site (see paragraph above). Rapidly adapting mechanoreceptive afferents are vigorously activated by vibration but not the nylon filaments; thus the disparity could reflect differences in this system. There is also evidence that individuals with autism process dynamic sensory information differently (Milne et al., 2002
), particularly when it is higher in complexity than comparison stimuli (Bertone, Mottron, Jelenic, & Faubert, 2003
), as is the case with vibrotactile as compared to light touch stimuli.
Since the hairy skin of the forearm is more often stimulated in the context of affiliative touch than the glabrous skin of the palm, which is specialized for fine haptic discrimination, this is an important finding to further characterize in autism. The forearm site was chosen in part because of its innervation by CT afferents, which is posited to constitute a social or affiliative touch system (Olausson et al., 2002
; Vallbo et al., 1999
; Wessberg et al., 2003
). However, it is unclear whether the effect seen in the present study can be ascribed to CT afferents, since (a) myelinated mechanoreceptive afferents also innervate the forearm and underlie discriminative sensitivity, and (b) CT afferents do not respond optimally to vibrotactile stimuli, instead responding preferentially to slow, stroking stimuli such as the textures used in Experiment 3.
Contrary to our hypothesis, in Experiment 3 we did not find a significant effect of group or a significant interaction between group and site on the pleasantness ratings of textures. This argues against a role for CT afferents in tactile hypersensitivity in autism, and needs to be reconciled with the findings in Experiment 2. We did note a small, nonsignificant, but consistent trend for individuals with autism to rate each of the textures overall as more pleasant than controls (see ). If verified by further investigation, this effect may provide insights into some of the sensory seeking behaviors that are characteristic of some individuals with autism. Idiosyncratic sensory stimuli (such as a flickering light or the texture of a certain material) may be unusually rewarding, and thus an individual with autism may pursue these sensory experiences repeatedly or fixate upon them to the neglect of other events in the environment. It would be of interest to uncover neural mechanisms underlying sensory seeking behaviors, which are often disruptive to the daily lives of individuals with autism and their families. Furthermore, utilizing sensory rewards (i.e., stimuli perceived to be particularly pleasant) may be useful for practitioners planning individualized interventions for persons with autism.
A limitation of Experiment 3 is in the nonsocial nature of the texture stimuli used. The perceptual and neural basis of social (interpersonal) touch is a current area of investigation; future studies should incorporate methodologies that specifically target the social context in which tactile hypersensitivity seems to occur most often in autism (Baranek, 1999
; Grandin, 2000
While no group differences were apparent in the detection of innocuous thermal stimuli (), there were significant group differences in thresholds for both heat and cold painful stimuli, as hypothesized (). In both cases, the autism group showed a greater degree of pain sensitivity, that is, their cold and heat pain thresholds were lower relative to the control group (i.e., cold pain was perceived at higher temperatures and heat pain at lower temperatures). In addition, sensitivity to heat pain also exhibited an interaction between group and session. The autism group was more sensitive to heat pain during the first session compared to the second session, while the average threshold of the control group remained stable over the two sessions (). Individuals with autism may have been more anxious about the unknown element of the heat pain stimulus, responding prematurely in the first session. Familiarity with the stimuli in the second session may have alleviated this anxiety in the second session, while controls may not have experienced this differential anxiety across sessions. However, it is unlikely that our results can be purely attributed to anxiety, as there was an overall group effect. In addition, there was a significant difference in cold pain sensitivity between the two groups, without an interaction between group and session, indicating that both cognitive and perceptual effects mediated hypersensitivity to thermal pain in the autism group.
In summary, this study demonstrates that high-functioning individuals with autism display normal tactile perception in light touch sensitivity, vibrotactile detection on the palm, vibrotactile adaptation, and innocuous thermal sensation, but significantly increased sensitivity to noxious thermal stimulation, and also to low-frequency vibration on the forearm. In addition, persons with autism tended to rate textures as more pleasant than controls. The group differences reflect the possibility of C-fiber involvement, but the study is limited by a relatively small sample size, and thus it is possible that negative findings partially reflect a lack of power. One cannot rule out the possibility that the positive findings are due to chance given the large number of tests performed, but we find it unlikely for two reasons: (1) two of the three significant findings were for painful stimuli which would be surprising if due to chance, and (2) the magnitude of the third significant group difference (vibrotactile detection at the forearm) was very large (with the autism group’s average threshold 34% lower than controls) to be attributable to chance.
In addition, we considered the possibility that group averages might obscure differences if the autism group had thresholds that followed a bimodal distribution (i.e., a subset within the autism group with very low thresholds corresponding to hyperresponsiveness, and another with very high thresholds corresponding to hyporesponsiveness). However, as is evident from the figures, variation was similar between the two groups, and frequency histograms (not shown) of thresholds on each task were also similar. A much larger sample size would be needed to assess distributions of sensory thresholds in autism; this kind of study should be done in the future. The altered thresholds we note for pain and low-frequency vibration have implications for understanding neural mechanisms associated with sensory-perceptual phenomena reported in the autism literature, and may be important to research further. Future studies should explore the contexts in which altered pain and pleasantness somatosensory sensitivity is exhibited in autism, and investigate the neural basis of observed hypersensitivity in autism using techniques such as neuroimaging and electrophysiological recordings.
Although clear evidence for a role of CT afferents in tactile hypersensitivity in autism was not gained, these findings add to a growing literature describing normal and sometimes enhanced perceptual abilities in autism. While the CT afferent system presents an attractive hypothesis for altered tactile sensitivity in autism, it is clear that multiple sensory modalities are affected. Of the empirical studies of vision to date, many suggest that individuals with autism exhibit enhanced
perception of certain stimulus properties, specifically local, circumscribed properties of a visual stimulus (Shah & Frith, 1983
; Joliffe & Baron-Cohen, 1997
; Mottron et al., 2003
). An analogous finding in the auditory domain (Mottron et al., 2000
) reveals that individuals with autism have an advantage for discriminating local changes in a musical melody (changes from note to note), but are similar to controls in processing more global melodic changes. Our finding of enhanced discriminative abilities for vibration applied to the forearm and enhanced affective sensitivity to thermal pain are consistent with this body of literature.
Touch input from parents is ubiquitous during normal parent–infant interactions (Stack & Muir, 1990
), has significant effects on social attention within the infant–parent dyad (Gusella, Muir, & Tronick, 1988
; Roggman & Woodson, 1989
), and shapes infants’ affective and attentional responses in formative early social interaction (Stack & Muir, 1992
). An early developmental abnormality in processing this information is likely to have far-reaching socio-cognitive effects throughout the lifespan. Alternatively, sensory abnormalities may be secondary to other symptoms of autism. The tendency toward social isolation may severely restrict somatosensory input in early development, leading to altered neural organization within somatosensory cortex. The immense capacity for experience-dependent plasticity of the somatosensory cortex has been demonstrated in both human (Merzenich & Jenkins, 1993
) and nonhuman primates (Elbert, Pantev, Wienbruch, Rockstroh, & Taub, 1995
; Sterr et al., 1998
Further psychophysical investigation of sensory abilities in autism is required to clarify the roles of sensation, perception and affect in autism. Another important step will be determining how to apply experimental methodology such as that employed in this study to younger people with autism, as sensory symptoms are known to change throughout development in autism (Kern et al., 2006
). However mixed the experimental results may be at this point, altered sensitivity in autism is very real to those individuals who experience it, and often interferes with daily life activities. It is important to continue searching for the source of these hyper/hyposensitivities in order to inform development of efficacious environmental adaptations and other interventions to maximize coping, optimal functioning, and social participation for individuals with autism whose lives are affected by sensory sensitivities.