Weaker neural suppression in autism.

Abnormal sensory processing has been observed in autism, including superior visual motion discrimination, but the neural basis for these sensory changes remains unknown. Leveraging well-characterized suppressive neural circuits in the visual system, we used behavioral and fMRI tasks to demonstrate a significant reduction in neural suppression in young adults with autism spectrum disorder (ASD) compared to neurotypical controls. MR spectroscopy measurements revealed no group differences in neurotransmitter signals. We show how a computational model that incorporates divisive normalization, as well as narrower top-down gain (that could result, for example, from a narrower window of attention), can explain our observations and divergent previous findings. Thus, weaker neural suppression is reflected in visual task performance and fMRI measures in ASD, and may be attributable to differences in top-down processing.

Reduced auditory cortical adaptation in autism spectrum disorder.

Adaptation is a fundamental property of cortical neurons and has been suggested to be altered in individuals with autism spectrum disorder (ASD). We used fMRI to measure adaptation induced by repeated audio-visual stimulation in early sensory cortical areas in individuals with ASD and neurotypical (NT) controls. The initial transient responses were equivalent between groups in both visual and auditory cortices and when stimulation occurred with fixed-interval and randomized-interval timing. However, in auditory but not visual cortex, the post-transient sustained response was greater in individuals with ASD than NT controls in the fixed-interval timing condition, reflecting reduced adaptation. Further, individual differences in the sustained response in auditory cortex correlated with ASD symptom severity. These findings are consistent with hypotheses that ASD is associated with increased neural responsiveness but that responsiveness differences only manifest after repeated stimulation, are specific to the temporal pattern of stimulation, and are confined to specific cortical regions.

Suppression and facilitation of human neural responses.

Efficient neural processing depends on regulating responses through suppression and facilitation of neural activity. Utilizing a well-known visual motion paradigm that evokes behavioral suppression and facilitation, and combining five different methodologies (behavioral psychophysics, computational modeling, functional MRI, pharmacology, and magnetic resonance spectroscopy), we provide evidence that challenges commonly held assumptions about the neural processes underlying suppression and facilitation. We show that: (1) both suppression and facilitation can emerge from a single, computational principle - divisive normalization; there is no need to invoke separate neural mechanisms, (2) neural suppression and facilitation in the motion-selective area MT mirror perception, but strong suppression also occurs in earlier visual areas, and (3) suppression is not primarily driven by GABA-mediated inhibition. Thus, while commonly used spatial suppression paradigms may provide insight into neural response magnitudes in visual areas, they should not be used to infer neural inhibition.

Spatial frequency selection and integration of global and local information in visual processing: A selective review and tribute to Shlomo Bentin.

Previous research has suggested a relationship between processing lower versus higher spatial frequencies (SFs) and global/local perception, respectively. Here we honor Shlomo Bentin by reviewing the work we conducted with him regarding this issue. This work was aimed at investigating the mechanisms by which selective attention to spatial frequency (SF) mediates global and local perception in general and how these perceptual levels are integrated with the shapes that define them. The experiments demonstrate that attention to global and local aspects of a hierarchical display biases the flexible selection of relatively lower and relatively higher SFs during image processing. Additionally, attentional selection of SF allows for the shapes in a hierarchical display to be integrated with the level (global/local) at which they occur. The studies reviewed here provide strong evidence that the flexible, top-down selection of low-level SF channels mediates the perception of global and local elements of visual displays. The studies also support a hemisphere asymmetry in this process, with right hemisphere functions biased toward global perception and left hemisphere functions biased toward local.

Attention Determines Contextual Enhancement versus Suppression in Human Primary Visual Cortex.

Neural responses in primary visual cortex (V1) depend on stimulus context in seemingly complex ways. For example, responses to an oriented stimulus can be suppressed when it is flanked by iso-oriented versus orthogonally oriented stimuli but can also be enhanced when attention is directed to iso-oriented versus orthogonal flanking stimuli. Thus the exact same contextual stimulus arrangement can have completely opposite effects on neural responses-in some cases leading to orientation-tuned suppression and in other cases leading to orientation-tuned enhancement. Here we show that stimulus-based suppression and enhancement of fMRI responses in humans depends on small changes in the focus of attention and can be explained by a model that combines feature-based attention with response normalization. SIGNIFICANCE STATEMENT: Neurons in the primary visual cortex (V1) respond to stimuli within a restricted portion of the visual field, termed their "receptive field." However, neuronal responses can also be influenced by stimuli that surround a receptive field, although the nature of these contextual interactions and underlying neural mechanisms are debated. Here we show that the response in V1 to a stimulus in the same context can either be suppressed or enhanced depending on the focus of attention. We are able to explain the results using a simple computational model that combines two well established properties of visual cortical responses: response normalization and feature-based enhancement.

Feature-based attention modulates surround suppression.

Stimuli appearing in the surround of the classical receptive field (CRF) can reduce neuronal firing and perceived contrast of a preferred stimulus in the CRF, a phenomenon referred to as surround suppression. Suppression is greatest when the surrounding stimulus has the same orientation and spatial frequency (SF) as the central target. Although spatial attention has been shown to influence surround suppression, the effects of feature-based attention have yet to be characterized. Using behavioral contrast adaptation in humans, we examined center-surround interactions between SF and orientation, and asked whether attending to one feature dimension versus the other influenced suppression. A center-surround triplet comprised of a central target Gabor and two flanking Gabors were used for adaptation. The flankers could have the same SF and orientation as the target, or differ in one or both of the feature dimensions. Contrast thresholds were measured for the target before and after adapting to center-surround triplets, and postadaptation thresholds were taken as an indirect measure of surround suppression. Both feature dimensions contributed to surround suppression and did not summate. Moreover, when center and surround had the same feature value in one dimension (e.g., same orientation) but had different values in the other dimension (e.g., different SF), there was more suppression when attention was directed to the feature dimension that matched between center and surround than when attention was directed to the feature dimension that differed. These results demonstrate that feature-based attention can influence center-surround interactions by enhancing the effects of the attended dimension.

Attending to global versus local stimulus features modulates neural processing of low versus high spatial frequencies: an analysis with event-related brain potentials.

Spatial frequency (SF) selection has long been recognized to play a role in global and local processing, though the nature of the relationship between SF processing and global/local perception is debated. Previous studies have shown that attention to relatively lower SFs facilitates global perception, and that attention to relatively higher SFs facilitates local perception. Here we recorded event-related brain potentials (ERPs) to investigate whether processing of low versus high SFs is modulated automatically during global and local perception, and to examine the time course of any such effects. Participants compared bilaterally presented hierarchical letter stimuli and attended to either the global or local levels. Irrelevant SF grating probes flashed at the center of the display 200 ms after the onset of the hierarchical letter stimuli could either be low or high in SF. It was found that ERPs elicited by the SF grating probes differed as a function of attended level (global versus local). ERPs elicited by low SF grating probes were more positive in the interval 196-236 ms during global than local attention, and this difference was greater over the right occipital scalp. In contrast, ERPs elicited by the high SF gratings were more positive in the interval 250-290 ms during local than global attention, and this difference was bilaterally distributed over the occipital scalp. These results indicate that directing attention to global versus local levels of a hierarchical display facilitates automatic perceptual processing of low versus high SFs, respectively, and this facilitation is not limited to the locations occupied by the hierarchical display. The relatively long latency of these attention-related ERP modulations suggests that initial (early) SF processing is not affected by attention to hierarchical level, lending support to theories positing a higher level mechanism to underlie the relationship between SF processing and global versus local perception.

Orientation-specific surround suppression in the primary visual cortex varies as a function of autistic tendency.

Individuals with autism spectrum disorder (ASD) exhibit superior performance on tasks that rely on local details in an image, and they exhibit deficits in tasks that require integration of local elements into a unified whole. These perceptual abnormalities have been proposed to underlie many of the characteristic features of ASD, but the underlying neural mechanisms are poorly understood. Here, we investigated the degree to which orientation-specific surround suppression, a well-known form of contextual modulation in visual cortex, is associated with autistic tendency in neurotypical (NT) individuals. Surround suppression refers to the phenomenon that the response to a stimulus in the receptive field of a neuron is suppressed when it is surrounded by stimuli just outside the receptive field. The suppression is greatest when the center and surrounding stimuli share perceptual features such as orientation. Surround suppression underlies a number of fundamental perceptual processes that are known to be atypical in individuals with ASD, including perceptual grouping and perceptual pop-out. However, whether surround suppression in the primary visual cortex (V1) is related to autistic traits has not been directly tested before. We used fMRI to measure the neural response to a center Gabor when it was surrounded by Gabors having the same or orthogonal orientation, and calculated a suppression index (SI) for each participant that denoted the magnitude of suppression in the same vs. orthogonal conditions. SI was positively correlated with degree of autistic tendency in each individual, as measured by the Autism Quotient (AQ) scale, a questionnaire designed to assess autistic traits in the general population. Age also correlated with SI and with autistic tendency in our sample, but did not account for the correlation between SI and autistic tendency. These results suggest a reduction in orientation-specific surround suppression in V1 with increasing autistic tendency.

Neural substrates of perceptual integration during bistable object perception.

The way we perceive an object depends both on feedforward, bottom-up processing of its physical stimulus properties and on top-down factors such as attention, context, expectation, and task relevance. Here we compared neural activity elicited by varying perceptions of the same physical image--a bistable moving image in which perception spontaneously alternates between dissociated fragments and a single, unified object. A time-frequency analysis of EEG changes associated with the perceptual switch from object to fragment and vice versa revealed a greater decrease in alpha (8-12 Hz) accompanying the switch to object percept than to fragment percept. Recordings of event-related potentials elicited by irrelevant probes superimposed on the moving image revealed an enhanced positivity between 184 and 212 ms when the probes were contained within the boundaries of the perceived unitary object. The topography of the positivity (P2) in this latency range elicited by probes during object perception was distinct from the topography elicited by probes during fragment perception, suggesting that the neural processing of probes differed as a function of perceptual state. Two source localization algorithms estimated the neural generator of this object-related difference to lie in the lateral occipital cortex, a region long associated with object perception. These data suggest that perceived objects attract attention, incorporate visual elements occurring within their boundaries into unified object representations, and enhance the visual processing of elements occurring within their boundaries. Importantly, the perceived object in this case emerged as a function of the fluctuating perceptual state of the viewer.

Attentional selection of relative SF mediates global versus local processing: evidence from EEG.

Previous research on functional hemispheric differences in visual processing has associated global perception with low spatial frequency (LSF) processing biases of the right hemisphere (RH) and local perception with high spatial frequency (HSF) processing biases of the left hemisphere (LH). The Double Filtering by Frequency (DFF) theory expanded this hypothesis by proposing that visual attention selects and is directed to relatively LSFs by the RH and relatively HSFs by the LH, suggesting a direct causal relationship between SF selection and global versus local perception. We tested this idea in the current experiment by comparing activity in the EEG recorded at posterior right and posterior left hemisphere sites while participants' attention was directed to global or local levels of processing after selection of relatively LSFs versus HSFs in a previous stimulus. Hemispheric asymmetry in the alpha band (8-12 Hz) during preparation for global versus local processing was modulated by the selected SF. In contrast, preparatory activity associated with selection of SF was not modulated by the previously attended level (global/local). These results support the DFF theory that top-down attentional selection of SF mediates global and local processing.

Shifting attention in viewer- and object-based reference frames after unilateral brain injury.

The aims of the present study were to investigate the respective roles that object- and viewer-based reference frames play in reorienting visual attention, and to assess their influence after unilateral brain injury. To do so, we studied 16 right hemisphere injured (RHI) and 13 left hemisphere injured (LHI) patients. We used a cueing design that manipulates the location of cues and targets relative to a display comprised of two rectangles (i.e., objects). Unlike previous studies with patients, we presented all cues at midline rather than in the left or right visual fields. Thus, in the critical conditions in which targets were presented laterally, reorienting of attention was always from a midline cue. Performance was measured for lateralized target detection as a function of viewer-based (contra- and ipsilesional sides) and object-based (requiring reorienting within or between objects) reference frames. As expected, contralesional detection was slower than ipsilesional detection for the patients. More importantly, objects influenced target detection differently in the contralesional and ipsilesional fields. Contralesionally, reorienting to a target within the cued object took longer than reorienting to a target in the same location but in the uncued object. This finding is consistent with object-based neglect. Ipsilesionally, the means were in the opposite direction. Furthermore, no significant difference was found in object-based influences between the patient groups (RHI vs. LHI). These findings are discussed in the context of reference frames used in reorienting attention for target detection.

Priming global and local processing of composite faces: revisiting the processing-bias effect on face perception.

We used the composite-face illusion and Navon stimuli to determine the consequences of priming local or global processing on subsequent face recognition. The composite-face illusion reflects the difficulty of ignoring the task-irrelevant half-face while attending the task-relevant half if the half-faces in the composite are aligned. On each trial, participants first matched two Navon stimuli, attending to either the global or the local level, and then matched the upper halves of two composite faces presented sequentially. Global processing of Navon stimuli increased the sensitivity to incongruence between the upper and the lower halves of the composite face, relative to a baseline in which the composite faces were not primed. Local processing of Navon stimuli did not influence the sensitivity to incongruence. Although incongruence induced a bias toward different responses, this bias was not modulated by priming. We conclude that global processing of Navon stimuli augments holistic processing of the face.

Attention to hierarchical level influences attentional selection of spatial scale.

Ample evidence suggests that global perception may involve low spatial frequency (LSF) processing and that local perception may involve high spatial frequency (HSF) processing (Shulman, Sullivan, Gish, & Sakoda, 1986; Shulman & Wilson, 1987; Robertson, 1996). It is debated whether SF selection is a low-level mechanism associating global and local information with absolute LSF and HSF content, or whether it is a higher level mechanism involving a selective process that defines the SF range in which global and local can then be relatively defined. The present study provides support for the latter claim by demonstrating that allocating attention to global or local levels of hierarchical displays biased selection of LSFs or HSFs, respectively, in subsequently presented compound gratings. This bias occurred despite a change in the response dimension (from letter identification in the hierarchical stimulus to orientation discrimination in the grating) and despite a difference in retinal location of the hierarchical stimuli and the grating stimulus. Moreover, the bias was determined by the relationship between the 2 SFs in the compound grating (i.e., their relative frequency) rather than the absolute SF values.

Local or global? Attentional selection of spatial frequencies binds shapes to hierarchical levels.

Contrary to the traditional view that shapes and their hierarchical level (local or global) are a priori integrated in perception, recent evidence suggests that the identity of a shape and its level are encoded independently, implying the need for shape-level binding to account for normal perception. What is the binding mechanism in this case? Using hierarchically arranged letter shapes, we obtained evidence that the left hemisphere has a preference for binding shapes to the local level, whereas the right hemisphere has a preference for binding shapes to the global level. More important, binding is modulated by attentional selection of higher or lower spatial frequencies. Attention to higher spatial frequencies facilitated subsequent binding by the left hemisphere of elements to the local level, whereas attention to lower spatial frequencies facilitated subsequent binding by the right hemisphere of elements to the global level.

Visual hemispatial neglect, re-assessed.

Increased computer use in clinical settings offers an opportunity to develop new neuropsychological tests that exploit the control computers have over stimulus dimensions and timing. However, before adopting new tools, empirical validation is necessary. In the current study, our aims were twofold: to describe a computerized adaptive procedure with broad potential for neuropsychological investigations, and to demonstrate its implementation in testing for visual hemispatial neglect. Visual search results from adaptive psychophysical procedures are reported from 12 healthy individuals and 23 individuals with unilateral brain injury. Healthy individuals reveal spatially symmetric performance on adaptive search measures. In patients, psychophysical outcomes (as well as those from standard paper-and-pencil search tasks) reveal visual hemispatial neglect. Consistent with previous empirical studies of hemispatial neglect, lateralized impairments in adaptive conjunction search are greater than in adaptive feature search tasks. Furthermore, those with right hemisphere damage show greater lateralized deficits in conjunction search than do those with left hemisphere damage. We argue that adaptive tests, which automatically adjust to each individual's performance level, are efficient methods for both clinical evaluations and neuropsychological investigations and have the potential to detect subtle deficits even in chronic stages, when flagrant clinical signs have frequently resolved.

Using spatial frequency scales for processing face features and face configuration: an ERP analysis.

In the present study we examined the influence of spatial filtering on the N170-effect, a relatively early face-selective ERP difference associated with face detection. We compared modulation of the N170-effect using spatially filtered stimuli that either facilitated feature analysis or impeded configural analysis. The salience of inner face components was enhanced by presenting them in isolation. Configural processing was manipulated by face inversion. The N170-effects elicited by upright faces and isolated inner components were similar across low- and high-spatial frequency scales. In contrast, the inversion effect (enhanced N170 amplitude for inverted compared with upright faces) was only observed with broadband and low-spatial frequency stimuli. These findings demonstrate that the N170-effect can be influenced by both low- and high-spatial frequency channels. Moreover, they indicate that different configural manipulations (isolated features vs. face inversion) affect face detection in distinct ways, consistent with separate processing mechanisms for different types of configural encoding.

Attentional control parameters following parietal-lobe damage: evidence from normal subjects.

Attentional control involves the factors, or cognitive parameters, that determine which environmental inputs receive attention and which do not. Cognitive studies of attentional control have highlighted two general classes of control parameters, bottom-up (data driven or exogenous) parameters and top-down (goal driven or endogenous) parameters. Which of these control parameters is affected following parietal-lobe damage? In parietal-damaged patients, it is possible that a disorder in one control parameter (e.g. goal driven) would appear as a disorder in another parameter (e.g. data driven). To investigate the control parameters that might be affected in parietal patients, we simulated neglect in normal participants by disrupting data-driven information processing. When half of a computer monitor was degraded by translucent tracing paper while normal participants performed a cued spatial attention task (Experiment 1), the normal participants showed a pattern of results similar to patients with unilateral parietal-lobe damage--the so-called "disengage deficit." This pattern of results replicated when neutral attentional cues were included in the experiment (Experiment 2). However, the disengage deficit was not simulated in normal participants with predictive central symbolic cues (Experiment 3) or predictive peripheral cues (Experiment 4). Because perceptual degradation influences data-driven attentional control parameters, we suggest that these control parameters may be disrupted following parietal-lobe damage.

Exogenous spatial attention influences figure-ground assignment.

In a hierarchical stage account of vision, figure-ground assignment is thought to be completed before the operation of focal spatial attention. Results of previous studies have supported this account by showing that unpredictive, exogenous spatial precues do not influence figure-ground assignment, although voluntary attention can influence figure-ground assignment. However, in these studies, attention was not summoned directly to a region in a figure-ground display. In three experiments, we addressed the relationship between figure-ground assignment and visuospatial attention. In Experiment 1, we replicated the finding that exogenous precues do not influence figure-ground assignment when they direct attention outside of a figure-ground stimulus. In Experiment 2, we demonstrated that exogenous attention can influence figure-ground assignment if it is directed to one of the regions in a figure-ground stimulus. In Experiment 3, we demonstrated that exogenous attention can influence figure-ground assignment in displays that contain a Gestalt figure-ground cue; this result suggests that figure-ground processes are not entirely completed prior to the operation of focal spatial attention. Exogenous spatial attention acts as a cue for figure-ground assignment and can affect the outcome of figure-ground processes.