Atypicalities in Perceptual Adaptation in Autism Do Not Extend to Perceptual Causality

A recent study showed that adaptation to causal events (collisions) in adults caused subsequent events to be less likely perceived as causal. In this study, we examined if a similar negative adaptation effect for perceptual causality occurs in children, both typically developing and with autism. Previous studies have reported diminished adaptation for face identity, facial configuration and gaze direction in children with autism. To test whether diminished adaptive coding extends beyond high-level social stimuli (such as faces) and could be a general property of autistic perception, we developed a child-friendly paradigm for adaptation of perceptual causality. We compared the performance of 22 children with autism with 22 typically developing children, individually matched on age and ability (IQ scores). We found significant and equally robust adaptation aftereffects for perceptual causality in both groups. There were also no differences between the two groups in their attention, as revealed by reaction times and accuracy in a change-detection task. These findings suggest that adaptation to perceptual causality in autism is largely similar to typical development and, further, that diminished adaptive coding might not be a general characteristic of autism at low levels of the perceptual hierarchy, constraining existing theories of adaptation in autism.     

The dynamics of visual adaptation to faces

Several recent demonstrations using visual adaptation have revealed high-level aftereffects for complex patterns including faces. While traditional aftereffects involve perceptual distortion of simple attributes such as orientation or colour that are processed early in the visual cortical hierarchy, face adaptation affects perceived identity and expression, which are thought to be products of higher-order processing. And, unlike most simple aftereffects, those involving faces are robust to changes in scale, position and orientation between the adapting and test stimuli. These differences raise the question of how closely related face aftereffects are to traditional ones. Little is known about the build-up and decay of the face aftereffect, and the similarity of these dynamic processes to traditional aftereffects might provide insight into this relationship. We examined the effect of varying the duration of both the adapting and test stimuli on the magnitude of perceived distortions in face identity. We found that, just as with traditional aftereffects, the identity aftereffect grew logarithmically stronger as a function of adaptation time and exponentially weaker as a function of test duration. Even the subtle aspects of these dynamics, such as the power-law relationship between the adapting and test durations, closely resembled that of other aftereffects. These results were obtained with two different sets of face stimuli that differed greatly in their low-level properties. We postulate that the mechanisms governing these shared dynamics may be dissociable from the responses of feature-selective neurons in the early visual cortex.     

Using Effort to Measure Reward Value of Faces in Children with Autism

According to one influential account, face processing atypicalities in autism reflect reduced reward value of faces, which results in limited attention to faces during development and a consequent failure to acquire face expertise. Surprisingly, however, there is a paucity of work directly investigating the reward value of faces for individuals with autism and the evidence for diminished face rewards in this population remains equivocal. In the current study, we measured how hard children with autism would work to view faces, using an effortful key-press sequence, and whether they were sensitive to the differential reward value of attractive and unattractive faces. Contrary to expectations, cognitively able children with autism did not differ from typically developing children of similar age and ability in their willingness to work to view faces. Moreover, the effort expended was strongly positively correlated with facial attractiveness ratings in both groups of children. There was also no evidence of atypical reward values for other, less social categories (cars and inverted faces) in the children with autism. These results speak against the possibility that face recognition difficulties in autism are explained by atypical reward value of faces.     

Abnormal adaptive face-coding mechanisms in children with autism spectrum disorder

In low-level vision, exquisite sensitivity to variation in luminance is achieved by adaptive mechanisms that adjust neural sensitivity to the prevailing luminance level. In high-level vision, adaptive mechanisms contribute to our remarkable ability to distinguish thousands of similar faces [1]. A clear example of this sort of adaptive coding is the face-identity aftereffect [2, 3, 4, 5], in which adaptation to a particular face biases perception toward the opposite identity. Here we investigated face adaptation in children with autism spectrum disorder (ASD) by asking them to discriminate between two face identities, with and without prior adaptation to opposite-identity faces. The ASD group discriminated the identities with the same precision as did the age- and ability-matched control group, showing that face identification per se was unimpaired. However, children with ASD showed significantly less adaptation than did their typical peers, with the amount of adaptation correlating significantly with current symptomatology, and face aftereffects of children with elevated symptoms only one third those of controls. These results show that although children with ASD can learn a simple discrimination between two identities, adaptive face-coding mechanisms are severely compromised, offering a new explanation for previously reported face-perception difficulties [6, 7, 8] and possibly for some of the core social deficits in ASD [9, 10].     

Adaptation improves discrimination of face identity

Whether face adaptation confers any advantages to perceptual processing remains an open question. We investigated whether face adaptation can enhance the ability to make fine discriminations in the vicinity of the adapted face. We compared face discrimination thresholds in three adapting conditions: (i) same-face: where adapting and test faces were the same, (ii) different-face: where adapting and test faces differed, and (iii) baseline: where the adapting stimulus was a blank. Discrimination thresholds for morphed identity changes involving the adapted face (same-face) improved compared with those from both the baseline (no-adaptation) and different-face conditions. Since adapting to a face did not alter discrimination performance for other faces, this effect is selective for the facial identity that is adapted. These results indicate a form of gain control to heighten perceptual sensitivity in the vicinity of a currently viewed face, analogous to forms of adaptive gain control at lower levels of the visual system.     

Perceptual auditory aftereffects on voice identity using brief vowel stimuli

Humans can identify individuals from their voice, suggesting the existence of a perceptual representation of voice identity. We used perceptual aftereffects - shifts in perceived stimulus quality after brief exposure to a repeated adaptor stimulus - to further investigate the representation of voice identity in two experiments. Healthy adult listeners were familiarized with several voices until they reached a recognition criterion. They were then tested on identification tasks that used vowel stimuli generated by morphing between the different identities, presented either in isolation (baseline) or following short exposure to different types of voice adaptors (adaptation). Experiment 1 showed that adaptation to a given voice induced categorization shifts away from that adaptor's identity even when the adaptors consisted of vowels different from the probe stimuli. Moreover, original voices and caricatures resulted in comparable aftereffects, ruling out an explanation of identity aftereffects in terms of adaptation to low-level features. In Experiment 2, we show that adaptors with a disrupted configuration, i.e., altered fundamental frequency or formant frequencies, failed to produce perceptual aftereffects showing the importance of the preserved configuration of these acoustical cues in the representation of voices. These two experiments indicate a high-level, dynamic representation of voice identity based on the combination of several lower-level acoustical features into a specific voice configuration.     

Dissociable Perceptual Effects of Visual Adaptation

Neurons in the visual cortex are responsive to the presentation of oriented and curved line segments, which are thought to act as primitives for the visual processing of shapes and objects. Prolonged adaptation to such stimuli gives rise to two related perceptual effects: a slow change in the appearance of the adapting stimulus (perceptual drift), and the distortion of subsequently presented test stimuli (adaptational aftereffects). Here we used a psychophysical nulling technique to dissociate and quantify these two classical observations in order to examine their underlying mechanisms and their relationship to one another. In agreement with previous work, we found that during adaptation horizontal and vertical straight lines serve as attractors for perceived orientation and curvature. However, the rate of perceptual drift for different stimuli was not predictive of the corresponding aftereffect magnitudes, indicating that the two perceptual effects are governed by distinct neural processes. Finally, the rate of perceptual drift for curved line segments did not depend on the spatial scale of the stimulus, suggesting that its mechanisms lie outside strictly retinotopic processing stages. These findings provide new evidence that the visual system relies on statistically salient intrinsic reference stimuli for the processing of visual patterns, and point to perceptual drift as an experimental window for studying the mechanisms of visual perception.     

Position specificity of adaptation-related face aftereffects

It has been shown that prolonged exposure to a human face leads to shape-selective visual aftereffects. It seems that these face-specific aftereffects (FAEs) have multiple components, related to the adaptation of earlier and higher level processing of visual stimuli. The largest magnitude of FAE, using long-term adaptation periods, is usually observed at the retinotopic position of the preceding adaptor stimulus. However, FAE is also detected, to a smaller degree, at other retinal positions in a spatially invariant way and this component depends less on the adaptation duration. Several lines of evidences suggest that while the position-specific FAE involves lower level areas of the ventral processing stream, the position-invariant FAE depends on the activation of higher level face-processing areas and the fusiform gyrus in particular. In the present paper, we summarize the available behavioural, electrophysiological and neuroimaging results regarding the spatial selectivity of FAE and discuss their implications for the visual stability of object representations across saccadic eye movements.     

Adaptation Aftereffects in Vocal Emotion Perception Elicited by Expressive Faces and Voices

The perception of emotions is often suggested to be multimodal in nature, and bimodal as compared to unimodal (auditory or visual) presentation of emotional stimuli can lead to superior emotion recognition. In previous studies, contrastive aftereffects in emotion perception caused by perceptual adaptation have been shown for faces and for auditory affective vocalization, when adaptors were of the same modality. By contrast, crossmodal aftereffects in the perception of emotional vocalizations have not been demonstrated yet. In three experiments we investigated the influence of emotional voice as well as dynamic facial video adaptors on the perception of emotion-ambiguous voices morphed on an angry-to-happy continuum. Contrastive aftereffects were found for unimodal (voice) adaptation conditions, in that test voices were perceived as happier after adaptation to angry voices, and vice versa. Bimodal (voice + dynamic face) adaptors tended to elicit larger contrastive aftereffects. Importantly, crossmodal (dynamic face) adaptors also elicited substantial aftereffects in male, but not in female participants. Our results (1) support the idea of contrastive processing of emotions (2), show for the first time crossmodal adaptation effects under certain conditions, consistent with the idea that emotion processing is multimodal in nature, and (3) suggest gender differences in the sensory integration of facial and vocal emotional stimuli.     

Luminance- and Texture-Defined Information Processing in School-Aged Children with Autism

According to the complexity-specific hypothesis, the efficacy with which individuals with autism spectrum disorder (ASD) process visual information varies according to the extensiveness of the neural network required to process stimuli. Specifically, adults with ASD are less sensitive to texture-defined (or second-order) information, which necessitates the implication of several cortical visual areas. Conversely, the sensitivity to simple, luminance-defined (or first-order) information, which mainly relies on primary visual cortex (V1) activity, has been found to be either superior (static material) or intact (dynamic material) in ASD. It is currently unknown if these autistic perceptual alterations are present in childhood. In the present study, behavioural (threshold) and electrophysiological measures were obtained for static luminance- and texture-defined gratings presented to school-aged children with ASD and compared to those of typically developing children. Our behavioural and electrophysiological (P140) results indicate that luminance processing is likely unremarkable in autistic children. With respect to texture processing, there was no significant threshold difference between groups. However, unlike typical children, autistic children did not show reliable enhancements of brain activity (N230 and P340) in response to texture-defined gratings relative to luminance-defined gratings. This suggests reduced efficiency of neuro-integrative mechanisms operating at a perceptual level in autism. These results are in line with the idea that visual atypicalities mediated by intermediate-scale neural networks emerge before or during the school-age period in autism.     

Perception of approaching and withdrawing sound sources after exposure to broadband noise: The importance of spatial domain

The existence of space-specific differences in auditory aftereffects has been tested under short-term (5 s) exposure to broadband noise (20–20000 Hz). Adapting stimuli were emitted as constant-amplitude noise sequences. Test stimuli could be of constant and changing amplitude: increasing amplitude of noise pulses in a sequence mimicked an approaching sound source, whereas a decrease in amplitude was perceived as withdrawal. The experiments were done in an anechoic chamber. Auditory aftereffects were assessed under the following conditions: (a) adapting and test stimuli were emitted through a loudspeaker mounted at a distance of 1.1 m from the listener (i.e., subjectively near); (b) both stimuli were emitted from a distance of 4.5 m (subjectively far); (c) adapting and test stimuli were emitted from different distances. The results showed that the characteristics of perception of the imitated sound source motion were similar in proximity and remoteness, which was observed both in the control (without adaptation) and after adaptation to noise. In the absence of adaptation, the psychophysical curves were asymmetrical: the listeners reported approaching of test stimuli more often for both spatial domains. However, the overestimation of test stimuli as drawing closer was more pronounced when they were emitted from the distance of 1.1 m, i.e., from near the listener. After the adaptation to noise, the aftereffects showed spatial specificity and were observed only when adapting and test stimuli belonged to the same spatial domain. These aftereffects were similar in their pattern and strength both in proximity and remoteness: the listeners reported withdrawal of test stimuli more frequently as compared with the control. As a result of these aftereffects, the symmetry of psychometric curves was restored, and the estimation of the direction of sound source motion in the experiment became equiprobable.     

Auditory aftereffects of approaching and withdrawing sound sources: Dependence on the trajectory and location of adapting stimuli

Perception of approaching and withdrawing sound sources and their action on auditory aftereffects were studied in the free field. Motion of adapting stimuli was mimicked in two ways: (1) simultaneous opposite changes of amplitude of broadband noise impulses at two loudspeakers placed at 1.1 and 4.5 m from the listener; (2) an increase or a decrease of amplitude of broadband noise impulses in only one loudspeaker, the nearer or the remote one. Motion of test stimuli was mimicked in the former way. Listeners determined direction of the test stimuli motion without any adaptation (control) or after adaptation to stationary, slowly moving (with an amplitude change of 2 dB) and rapidly moving (amplitude change of 12 dB) stimuli. Percentages of “withdrawal” reports were used for construction of psychometric curves. Three phenomena of auditory perception were observed. In the absence of adaptation, a growing-louder effect was revealed, i.e., listeners reported more frequently the test sounds as the approaching ones. Once adapted to stationary or slowly moving stimuli, listeners showed a location-dependent aftereffect. Test stimuli were reported as withdrawing more often as compared with control. The effect was associated with the previous one and was weaker when the distance to the loudspeaker producing adapting stimuli was greater. After adaptation to rapidly moving stimuli, a motion aftereffect was revealed. In this case, listeners reported a direction of test stimuli motion as being opposite to that of adapting stimuli. The motion aftereffect was more pronounced when the adapting stimuli motion was mimicked in the former way, as this method allows estimation of their trajectory. There was no relationship between the motion aftereffect and the growing-louder effect, whichever way the adapting stimuli were produced. There was observed a tendency for reduction of aftereffects of approaching and for intensification of aftereffects of withdrawal with growing distance from source of adapting stimuli.     

Point Me in the Right Direction: Same and Cross Category Visual Aftereffects to Directional Cues

Of the many hand gestures that we use in communication pointing is one of the most common and powerful in its role as a visual referent that directs joint attention. While numerous studies have examined the developmental trajectory of pointing production and comprehension, very little consideration has been given to adult visual perception of hand pointing gestures. Across two studies, we use a visual adaptation paradigm to explore the mechanisms underlying the perception of proto-declarative hand pointing. Twenty eight participants judged whether 3D modeled hands pointed, in depth, at or to the left or right of a target (test angles of 0°, 0.75° and 1.5° left and right) before and after adapting to either hands or arrows which pointed 10° to the right or left of the target. After adaptation, the perception of the pointing direction of the test hands shifted with respect to the adapted direction, revealing separate mechanisms for coding right and leftward pointing directions. While there were subtle yet significant differences in the strength of adaptation to hands and arrows, both cues gave rise to a similar pattern of aftereffects. The considerable cross category adaptation found when arrows were used as adapting stimuli and the asymmetry in aftereffects to left and right hands suggests that the adaptation aftereffects are likely driven by simple orientation cues, inherent in the morphological structure of the hand, and not dependent on the biological status of the hand pointing cue. This finding provides evidence in support of a common neural mechanism that processes these directional social cues, a mechanism that may be blind to the biological status of the stimulus category.     

Adaptor Identity Modulates Adaptation Effects in Familiar Face Identification and Their Neural Correlates

Adaptation-related aftereffects (AEs) show how face perception can be altered by recent perceptual experiences. Along with contrastive behavioural biases, modulations of the early event-related potentials (ERPs) were typically reported on categorical levels. Nevertheless, the role of the adaptor stimulus per se for face identity-specific AEs is not completely understood and was therefore investigated in the present study. Participants were adapted to faces (S1s) varying systematically on a morphing continuum between pairs of famous identities (identities A and B), or to Fourier phase-randomized faces, and had to match the subsequently presented ambiguous faces (S2s; 50/50% identity A/B) to one of the respective original faces. We found that S1s identical with or near to the original identities led to strong contrastive biases with more identity B responses following A adaptation and vice versa. In addition, the closer S1s were to the 50/50% S2 on the morphing continuum, the smaller the magnitude of the AE was. The relation between S1s and AE was, however, not linear. Additionally, stronger AEs were accompanied by faster reaction times. Analyses of the simultaneously recorded ERPs revealed categorical adaptation effects starting at 100 ms post-stimulus onset, that were most pronounced at around 125–240 ms for occipito-temporal sites over both hemispheres. S1-specific amplitude modulations were found at around 300–400 ms. Response-specific analyses of ERPs showed reduced voltages starting at around 125 ms when the S1 biased perception in a contrastive way as compared to when it did not. Our results suggest that face identity AEs do not only depend on physical differences between S1 and S2, but also on perceptual factors, such as the ambiguity of S1. Furthermore, short-term plasticity of face identity processing might work in parallel to object-category processing, and is reflected in the first 400 ms of the ERP.     

Tilt aftereffects generated by bilaterally symmetrical patterns

Tilt aftereffects were generated by bilaterally symmetrical dot patterns. Both expansion and contraction effects, similar in size and magnitude to effects usually reported with luminance contours, were observed after adaptation to symmetrical patterns tilted 15 deg or 75 deg respectively from a vertically oriented test. Large effects were found when both adapting and test stimuli were symmetrical patterns while smaller effects were found when the adapting stimulus was symmetrical and test stimulus was a grating. A third experiment, which manipulated the number of dots near the axis line, confirmed the above findings; expansion and contraction effects were observed again. The results of these experiments suggest that the neural mechanism underlying the perception of luminance contours may be linked to the mechanism for the detection of symmetry.     

Tactile Motion Adaptation Reduces Perceived Speed but Shows No Evidence of Direction Sensitivity

Introduction

While the directionality of tactile motion processing has been studied extensively, tactile speed processing and its relationship to direction is little-researched and poorly understood. We investigated this relationship in humans using the ‘tactile speed aftereffect’ (tSAE), in which the speed of motion appears slower following prolonged exposure to a moving surface.

Method

We used psychophysical methods to test whether the tSAE is direction sensitive. After adapting to a ridged moving surface with one hand, participants compared the speed of test stimuli on the adapted and unadapted hands. We varied the direction of the adapting stimulus relative to the test stimulus.

Results

Perceived speed of the surface moving at 81 mms⁻¹ was reduced by about 30% regardless of the direction of the adapting stimulus (when adapted in the same direction, Mean reduction = 23 mms⁻¹, SD = 11; with opposite direction, Mean reduction = 26 mms⁻¹, SD = 9). In addition to a large reduction in perceived speed due to adaptation, we also report that this effect is not direction sensitive.

Conclusions

Tactile motion is susceptible to speed adaptation. This result complements previous reports of reliable direction aftereffects when using a dynamic test stimulus as together they describe how perception of a moving stimulus in touch depends on the immediate history of stimulation. Given that the tSAE is not direction sensitive, we argue that peripheral adaptation does not explain it, because primary afferents are direction sensitive with friction-creating stimuli like ours (thus motion in their preferred direction should result in greater adaptation, and if perceived speed were critically dependent on these afferents’ response intensity, the tSAE should be direction sensitive). The adaptation that reduces perceived speed therefore seems to be of central origin.     

Imagine Jane and identify John: face identity aftereffects induced by imagined faces

It is not known whether prolonged exposure to perceived and imagined complex visual images produces similar shifts in subsequent perception through selective adaptation. This question is important because a positive finding would suggest that perception and imagery of visual stimuli are mediated by shared neural networks. In this study, we used a selective adaptation procedure designed to induce high-level face-identity aftereffects--a phenomenon in which extended exposure to a particular face facilitates recognition of subsequent faces with opposite features while impairing recognition of all other faces. We report here that adaptation to either real or imagined faces produces a similar shift in perception and that identity boundaries represented in real and imagined faces are equivalent. Together, our results show that identity information contained in imagined and real faces produce similar behavioral outcomes. Our findings of high-level visual aftereffects induced by imagined stimuli can be taken as evidence for the involvement of shared neural networks that mediate perception and imagery of complex visual stimuli.     

Event-related Potential Study of Novelty Processing Abnormalities in Autism

To better understand visual processing abnormalities in autism we studied the attention orienting related frontal event potentials (ERP) and the sustained attention related centro-parietal ERPs in a three stimulus oddball experiment. The three stimulus oddball paradigm was aimed to test the hypothesis that individuals with autism abnormally orient their attention to novel distracters as compared to controls. A dense-array 128 channel EGI electroencephalographic (EEG) system was used on 11 high-functioning children and young adults with autism spectrum disorder (ASD) and 11 age-matched, typically developing control subjects. Patients with ASD showed slower reaction times but did not differ in response accuracy. At the anterior (frontal) topography the ASD group showed significantly higher amplitudes and longer latencies of early ERP components (e.g., P100, N100) to novel distracter stimuli in both hemispheres. The ASD group also showed prolonged latencies of late ERP components (e.g., P2a, N200, P3a) to novel distracter stimuli in both hemispheres. However, differences were more profound in the right hemisphere for both early and late ERP components. Our results indicate augmented and prolonged early frontal potentials and a delayed P3a component to novel stimuli, which suggest low selectivity in pre-processing and later-stage under-activation of integrative regions in the prefrontal cortices. Also, at the posterior (centro-parietal) topography the ASD group showed significantly prolonged N100 latencies and reduced amplitudes of the N2b component to target stimuli. In addition, the latency of the P3b component was prolonged to novel distracters in the ASD group. In general, the autistic group showed prolonged latencies to novel stimuli especially in the right hemisphere. These results suggest that individuals with autism over-process information needed for the successful differentiation of target and novel stimuli. We propose the potential application of ERP evaluations in a novelty task as outcome measurements in the biobehavioral treatment (e.g., EEG biofeedback, TMS) of autism.     

Shading and texture: separate information channels with a common adaptation mechanism?

We outline a scheme for the way in which early vision may handle information about shading (luminance modulation, LM) and texture (contrast modulation, CM). Previous work on the detection of gratings has found no sub-threshold summation, and no cross-adaptation, between LM and CM patterns. This strongly implied separate channels for the detection of LM and CM structure. However, we now report experiments in which adapting to LM (or CM) gratings creates tilt aftereffects of similar magnitude on both LM and CM test gratings, and reduces the perceived strength (modulation depth) of LM and CM gratings to a similar extent. This transfer of aftereffects between LM and CM might suggest a second stage of processing at which LM and CM information is integrated. The nature of this integration, however, is unclear and several simple predictions are not fulfilled. Firstly, one might expect the integration stage to lose identity information about whether the pattern was LM or CM. We show instead that the identity of barely detectable LM and CM patterns is not lost. Secondly, when LM and CM gratings are combined in-phase or out-of-phase we find no evidence for cancellation, nor for 'phase-blindness'. These results suggest that information about LM and CM is not pooled or merged--shading is not confused with texture variation. We suggest that LM and CM signals are carried by separate channels, but they share a common adaptation mechanism that accounts for the almost complete transfer of perceptual aftereffects.