Cortical synchronization suggests neural principles of visual feature grouping

Compositions of visual scenes are related here to neural signals in visual cortex and to cortical circuit models to understand neural mechanisms of perceptual feature grouping. Starting from the hypothesis that synchronization and decoupling of cortical gamma-activities (35-90 Hz) define the relations among visual objects, we concentrate on synchronization related to (1) static retinal stimulation during ocular fixation, and (2) transient stimulation by sudden shifts in object position. The synchronization hypothesis has been tested by analyzing signal correlations in visual cortex of monkeys with the following results: Static retinal stimuli induce loosely phase-coupled gamma-activities among neurons of an object's cortical representation. Patches of gamma-synchronization become decoupled across the representation of an object's contour, and thereby can code figure-ground segregation. Transient stimuli evoke synchronized volleys of stimulus-locked activities that are typically non-rhythmic and include low frequency components in addition to those in the gamma-range. It is argued that stimulus-induced and stimulus-locked synchronizations may play different roles in perceptual feature grouping.     

Stimulus context modulates competition in human extrastriate cortex

When multiple stimuli appear simultaneously in the visual field, they are not processed independently, but rather interact in a mutually suppressive way, suggesting that they compete for neural representation in visual cortex. The biased competition model of selective attention predicts that the competition can be influenced by both top-down and bottom-up mechanisms. Directed attention has been shown to bias competition in favor of the attended stimulus in extrastriate cortex. Here, we show that suppressive interactions among multiple stimuli are eliminated in extrastriate cortex when they are presented in the context of pop-out displays, in which a single item differs from the others, but not in heterogeneous displays, in which all items differ from each other. The pop-out effects seemed to originate in early visual cortex and were independent of attentional top-down control, suggesting that stimulus context may provide a powerful influence on neural competition in human visual cortex.     

Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice

Experience can shape cortical circuits, especially during critical periods for plasticity. In visual cortex, imbalance of activity from the two eyes during the critical period shifts ocular dominance (OD) towards the more active eye. Inhibitory circuits are crucial in this process: OD plasticity is absent in GAD65KO mice that show diminished inhibition. This defect can be rescued by application of benzodiazepines, which increase GABAergic signalling. However, it is unknown how such changes in inhibition might disrupt and then restore OD plasticity. Since NMDA dependent synaptic plasticity mechanisms are also known to contribute to OD plasticity, we investigated whether NMDA receptor levels and function are also altered in GAD65KO. There are reduced NR2A levels and slower NMDA currents in visual cortex of GAD65KO mice. Application of benzodiazepines, which rescues OD plasticity, also increases NR2A levels. Thus it appears as if OD plasticity can be restored by adding a critical amount of excitatory transmission through NR2A-containing NMDA receptors. Together, these observations can unify competing ideas of how OD plasticity is regulated: changes in either inhibition or excitation would engage homeostatic mechanisms that converge to regulate NMDA receptors, thereby enabling plasticity mechanisms and also ensuring circuit stability.     

Figure-ground mechanisms provide structure for selective attention

Attention depends on figure-ground organization: figures draw attention, whereas shapes of the ground tend to be ignored. Recent research has revealed mechanisms for figure-ground organization in the visual cortex, but how these mechanisms relate to the attention process remains unclear. Here we show that the influences of figure-ground organization and volitional (top-down) attention converge in single neurons of area V2 in Macaca mulatta. Although we found assignment of border ownership for attended and for ignored figures, attentional modulation was stronger when the attended figure was located on the neuron's preferred side of border ownership. When the border between two overlapping figures was placed in the receptive field, responses depended on the side of attention, and enhancement was generally found on the neuron's preferred side of border ownership. This correlation suggests that the neural network that creates figure-ground organization also provides the interface for the top-down selection process.     

Spatial attention enhances the selective integration of activity from area MT

Distinguishing which of the many proposed neural mechanisms of spatial attention actually underlies behavioral improvements in visually guided tasks has been difficult. One attractive hypothesis is that attention allows downstream neural circuits to selectively integrate responses from the most informative sensory neurons. This would allow behavioral performance to be based on the highest-quality signals available in visual cortex. We examined this hypothesis by asking how spatial attention affects both the stimulus sensitivity of middle temporal (MT) neurons and their corresponding correlation with behavior. Analyzing a data set pooled from two experiments involving four monkeys, we found that spatial attention did not appreciably affect either the stimulus sensitivity of the neurons or the correlation between their activity and behavior. However, for those sessions in which there was a robust behavioral effect of attention, focusing attention inside the neuron's receptive field significantly increased the correlation between these two metrics, an indication of selective integration. These results suggest that, similar to mechanisms proposed for the neural basis of perceptual learning, the behavioral benefits of focusing spatial attention are attributable to selective integration of neural activity from visual cortical areas by their downstream targets.     

Synchrony and covariation of firing rates in the primary visual cortex during contour grouping

The visual system imposes structure onto incoming information, by grouping image elements of a single object together, and by segregating them from elements that belong to other objects and the background. One influential theory holds that the code for grouping and segmentation is carried by the synchrony of neuronal discharges on a millisecond time scale. We tested this theory by recording neuronal activity in the primary visual cortex (area V1) of monkeys engaged in a contour-grouping task. We found that synchrony was unrelated to contour grouping. The firing rates of V1 neurons are also correlated across trials. We demonstrate that this rate covariation is mainly determined by fluctuations in visual attention. Moreover, we show that rate covariation depends on perceptual grouping, as it is strongest between neurons that respond to features of the same object.     

Delay activity and sensory-motor translation during planned eye or hand movements to visual or tactile targets

To perform eye or hand movements toward a relevant location, the brain must translate sensory input into motor output. Recent studies revealed segregation between circuits for translating visual information into saccadic or manual movements, but less is known about translation of tactile information into such movements. Using human functional magnetic resonance imaging (fMRI) in a delay paradigm, we factorially crossed sensory modality (vision or touch) and motor effector (eyes or hands) for lateralized movements (gaze shifts to left or right or pressing a left or right button with the corresponding left or right hand located there). We investigated activity in the delay-period between stimulation and response, asking whether the currently relevant side (left or right) during the delay was encoded according to sensory modality, upcoming motor response, or some interactive combination of these. Delay activity mainly reflected the motor response subsequently required. Irrespective of visual or tactile input, we found sustained activity in posterior partial cortex, frontal-eye field, and contralateral visual cortex when subjects would later make an eye movement. For delays prior to manual button-press response, activity increased in contralateral precentral regions, again regardless of stimulated modality. Posterior superior temporal sulcus showed sustained delay activity, irrespective of sensory modality, side, and response type. We conclude that the delay activations reflect translation of sensory signals into effector-specific motor circuits in parietal and frontal cortex (plus an impact on contralateral visual cortex for planned saccades), regardless of cue modality, whereas posterior STS provides a representation that generalizes across both sensory modality and motor effector.     

Predictive coding for motion stimuli in human early visual cortex

The current study investigates if early visual cortical areas, V1, V2 and V3, use predictive coding to process motion information. Previous studies have reported biased visual motion responses at locations where novel visual information was presented (i.e., the motion trailing edge), which is plausibly linked to the predictability of visual input. Using high-field functional magnetic resonance imaging (fMRI), we measured brain activation during predictable versus unpreceded motion-induced contrast changes during several motion stimuli. We found that unpreceded moving dots appearing at the trailing edge gave rise to enhanced BOLD responses, whereas predictable moving dots at the leading edge resulted in suppressed BOLD responses. Furthermore, we excluded biases in directional sensitivity, shifts in cortical stimulus representation, visuo-spatial attention and classical receptive field effects as viable alternative explanations. The results clearly indicate the presence of predictive coding mechanisms in early visual cortex for visual motion processing, underlying the construction of stable percepts out of highly dynamic visual input.     

Modality-independent role of the primary auditory cortex in time estimation

It has been argued that both modality-specific and supramodal mechanisms dedicated to time perception underlie the estimation of interval durations. While it is generally assumed that early sensory areas are dedicated to modality-specific time estimation, we hypothesized that early sensory areas such as the primary visual cortex or the auditory cortex might be involved in time perception independently of the sensory modality of the input. To test this possibility, we examined whether disruption of the primary visual cortex or the auditory cortex would disrupt time estimation of auditory stimuli and visual stimuli using transcranial magnetic stimulation (TMS). We found that disruption of the auditory cortex impaired not only time estimation of auditory stimuli but also impaired that of visual stimuli to the same degree. This finding suggests a supramodal role of the auditory cortex in time perception. On the other hand, TMS over the primary visual cortex impaired performance only in visual time discrimination. These asymmetric contributions of the auditory and visual cortices in time perception may be explained by a superiority of the auditory cortex in temporal processing. Here, we propose that time is primarily encoded in the auditory system and that visual inputs are automatically encoded into an auditory representation in time discrimination tasks.     

Contrast invariance of orientation tuning in cat primary visual cortex neurons depends on stimulus size

Key points

• The process of orientation tuning is an important and well‐characterized feature of neurons in primary visual cortex.
• The combination of ascending and descending circuits involved is not only relevant to understanding visual processing but the function of neocortex in general.
• The classic feed‐forward model of orientation tuning predicts a broadening effect due to increasing contrast; yet, experimental results consistently report contrast invariance.
• We show here that contrast invariance actually depends on stimulus size such that large stimuli extending beyond the neuron''s receptive field engage circuits that promote invariance, whereas optimally sized, smaller stimuli result in contrast variance that is more in line with the classical orientation tuning model.
• These results illustrate the importance of optimizing stimulus parameters to best reflect the sensory pathways under study and provide new clues about different circuits that may be involved in variant and invariant response properties.

Abstract

Selective response to stimulus orientation is a key feature of neurons in primary visual cortex, yet the underlying mechanisms generating orientation tuning are not fully understood. The combination of feed‐forward and cortical mechanisms involved is not only relevant to understanding visual processing but the function of neocortex in general. The classic feed‐forward model predicts that orientation tuning should broaden considerably with increasing contrast; however, experimental results consistently report contrast invariance. We show here, in primary visual cortex of anaesthetized cats under neuromuscular blockade, that contrast invariance occurs when visual stimuli are large enough to include the extraclassical surround (ECS), which is likely to involve circuits of suppression that may not be entirely feed‐forward in origin. On the other hand, when stimulus size is optimized to the classical receptive field of each neuron, the population average shows a statistically significant 40% increase in tuning width at high contrast, demonstrating that contrast variance of orientation tuning can occur. Conversely, our results also suggest that the phenomenon of contrast invariance relies in part on the presence of the ECS. Moreover, these results illustrate the importance of optimizing stimulus parameters to best reflect the neural pathways under study.

Abbreviations

CRF

classical receptive field

CV

circular variance

ECS

extraclassical receptive field

HWHH

half‐width at half‐height

LGN

lateral geniculate nucleus

V1

primary visual cortex

     

Active eye fixation performance in 940 young men: effects of IQ,schizotypy, anxiety and depression

Cortical activity depends on the balance between excitatory and inhibitory influences. Several different excitatory and inhibitory systems in the human motor cortex can be tested by transcranial magnetic stimulation (TMS). While considerable information is known about these different inhibitory and excitatory phenomena individually, how they are related to each other and how they interact is not well understood. Several recent studies have investigated the interactions between some of these circuits by applying them together. It has been found that short-interval intracortical inhibition (SICI) and long-interval intracortical inhibition (LICI) are mediated by different circuits. LICI appears to inhibit SICI, which may occur through presynaptic GABA_B receptors. Interhemispheric inhibition elicited by stimulation of the contralateral motor cortex also inhibits SICI and may share inhibitory mechanisms with LICI. Long-interval afferent inhibition induced by median nerve stimulation inhibits LICI but does not interact with SICI. Based on these results, a model of interactions between different inhibitory systems that can be tested and refined in the future is proposed. Further studies of the interaction between different cortical inhibitory and excitatory circuits should improve our understanding of the functional organization of the motor cortex and allow better interpretation of abnormal findings in disease states. It may also be developed into a new way of studying the pathophysiology of diseases and the effects of intervention.     

Selective Attention in Auditory Processing as Reflected by Event-Related Brain Potentials

Measures of event-related brain potentials (ERPs) have revealed two kinds of selective-attention mechanisms that operate on attended and unattended auditory stimuli. The processing negativity of the ERP reveals a mechanism of intramodal selective attention in the auditory cortex controlled by the frontal cortex. This mechanism selects attended auditory stimuli for further processing when they differ from unattended stimuli in location or tonal frequency. Studies of intermodal selective attention have compared auditory ERPs during auditory and visual attention. At least in part different brain mechanisms may be involved in the selection of auditory stimuli among other auditory stimuli (intramodal selective attention) and in the selection of auditory stimuli among visual stimuli (intermodal selective attention). This is suggested by the results showing that the earlier component of the processing negativity, which is generated in the auditory cortex during intramodal selective attention, differs in scalp distribution from the early attention-related negativity elicited during intermodal selective attention. With respect to the unattended auditory stimuli, ERP studies of selective attention suggest that physical features of these stimuli are extensively processed. This is shown by the mismatch negativity component of the ERP, which is usually elicited by infrequent physical deviations in an auditory stimulus sequence both when this sequence is attended and when it is ignored. This would be impossible if the physical stimulus features were not extensively processed, even in the absence of attention.     

Random visual noise impairs object-based attention

Object-based visual attention is observed when the benefit of attending to one element in a display extends to other elements that are part of the same perceptual object. Apperceptive agnosia is an object identification deficit in which spatial attention is preserved but object-based attention is impaired. Some debate exists regarding the extent to which the object-based impairment can be attributed to perceptual mechanisms that are specifically involved in grouping and segmentation of a scene, as opposed to early sensory processes. In the present paper we show that random visual noise is sufficient to eliminate the object benefit, a result inconsistent with the view that grouping mechanisms are responsible for the effect. The results have implications for an understanding of apperceptive agnosia, and for an understanding of object-based attention more generally.     

Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex

Recent in vitro studies have shown that acetylcholine (ACh) selectively reduces the efficacy of lateral cortical connections via a muscarinic mechanism, while boosting the efficacy of thalamocortical/feed-forward connections via a nicotinic mechanism. This suggests that high levels of ACh should reduce center-surround interactions of neurons in primary visual cortex, making cells more reliant on feed-forward information. In line with this hypothesis, we show that local iontophoretic application of ACh in primate primary visual cortex reduced the extent of spatial integration, assessed by recording a neurons' length tuning. When ACh was externally applied, neurons' preferred length shifted toward shorter bars, showing reduced impact of the extra-classical receptive field. We fitted a difference and a ratio of Gaussian model to these data to determine the underlying mechanisms of this dynamic change of spatial integration. These models assume overlapping summation and suppression areas with different widths and gains to be responsible for spatial integration and size tuning. ACh significantly reduced the extent of the summation area, but had no significant effect on the extent of the suppression area. In line with previous studies, we also show that applying ACh enhanced the response in the majority of cells, especially in the later (sustained) part of the response. These findings are similar to effects of attention on neuronal activity. The natural release of ACh is strongly linked with states of arousal and attention. Our results may therefore be relevant to the neurobiological mechanism of attention.     

Adaptive changes in early and late blind: a fMRI study of Braille reading.

Braille reading depends on remarkable adaptations that connect the somatosensory system to language. We hypothesized that the pattern of cortical activations in blind individuals reading Braille would reflect these adaptations. Activations in visual (occipital-temporal), frontal-language, and somatosensory cortex in blind individuals reading Braille were examined for evidence of differences relative to previously reported studies of sighted subjects reading print or receiving tactile stimulation. Nine congenitally blind and seven late-onset blind subjects were studied with fMRI as they covertly performed verb generation in response to reading Braille embossed nouns. The control task was reading the nonlexical Braille string "######". This study emphasized image analysis in individual subjects rather than pooled data. Group differences were examined by comparing magnitudes and spatial extent of activated regions first determined to be significant using the general linear model. The major adaptive change was robust activation of visual cortex despite the complete absence of vision in all subjects. This included foci in peri-calcarine, lingual, cuneus and fusiform cortex, and in the lateral and superior occipital gyri encompassing primary (V1), secondary (V2), and higher tier (VP, V4v, LO and possibly V3A) visual areas previously identified in sighted subjects. Subjects who never had vision differed from late blind subjects in showing even greater activity in occipital-temporal cortex, provisionally corresponding to V5/MT and V8. In addition, the early blind had stronger activation of occipital cortex located contralateral to the hand used for reading Braille. Responses in frontal and parietal cortex were nearly identical in both subject groups. There was no evidence of modifications in frontal cortex language areas (inferior frontal gyrus and dorsolateral prefrontal cortex). Surprisingly, there was also no evidence of an adaptive expansion of the somatosensory or primary motor cortex dedicated to the Braille reading finger(s). Lack of evidence for an expected enlargement of the somatosensory representation may have resulted from balanced tactile stimulation and gross motor demands during Braille reading of nouns and the control fields. Extensive engagement of visual cortex without vision is discussed in reference to the special demands of Braille reading. It is argued that these responses may represent critical language processing mechanisms normally present in visual cortex.     

Push-pull mechanism of selective attention in human extrastriate cortex

Selective attention operates in visual cortex by facilitating processing of selected stimuli and by filtering out unwanted information from nearby distracters over circumscribed regions of visual space. The neural representation of unattended stimuli outside this focus of attention is less well understood. We studied the neural fate of unattended stimuli using functional magnetic resonance imaging by dissociating the activity evoked by attended (target) stimuli presented to the periphery of a visual hemifield and unattended (distracter) stimuli presented simultaneously to a corresponding location of the contralateral hemifield. Subjects covertly directed attention to a series of target stimuli and performed either a low or a high attentional-load search task on a stream of otherwise identical stimuli. With this task, target-search-related activity increased with increasing attentional load, whereas distracter-related activity decreased with increasing load in areas V4 and TEO but not in early areas V1 and V2. This finding presents evidence for a load-dependent push-pull mechanism of selective attention that operates over large portions of the visual field at intermediate processing stages. This mechanism appeared to be controlled by a distributed frontoparietal network of brain areas that reflected processes related to target selection during spatially directed attention.     

Global motion mechanisms compensate local motion deficits in a patient with a bilateral occipital lobe lesion

Successive stages of cortical processing encode increasingly more complex types of information. In the visual motion system this increasing complexity, complemented by an increase in spatial summation, has proven effective in characterizing the mechanisms mediating visual perception. Here we report psychophysical results from a motion-impaired stroke patient, WB, whose pattern of deficits over time reveals a systematic shift in spatial scale for processing speed. We show that following loss in sensitivity to low-level motion direction WB’s representation of speed shifts to larger spatial scales, consistent with recruitment of intact high-level mechanisms. With the recovery of low-level motion processing WB’s representation of speed shifts back to small spatial scales. These results support the recruitment of high-level visual mechanisms in cases where lower-level function is impaired and suggest that, as an experimental paradigm, spatial summation may provide an important avenue for investigating functional recovery in patients following damage to visually responsive cortex.     

Transient neural activity in human parietal cortex during spatial attention shifts

Observers viewing a complex visual scene selectively attend to relevant locations or objects and ignore irrelevant ones. Selective attention to an object enhances its neural representation in extrastriate cortex, compared with those of unattended objects, via top-down attentional control signals. The posterior parietal cortex is centrally involved in this control of spatial attention. We examined brain activity during attention shifts using rapid, event-related fMRI of human observers as they covertly shifted attention between two peripheral spatial locations. Activation in extrastriate cortex increased after a shift of attention to the contralateral visual field and remained high during sustained contralateral attention. The time course of activity was substantially different in posterior parietal cortex, where transient increases in activation accompanied shifts of attention in either direction. This result suggests that activation of the parietal cortex is associated with a discrete signal to shift spatial attention, and is not the source of a signal to continuously maintain the current attentive state.     

The auditory cortex mediates the perceptual effects of acoustic temporal expectation

When events occur at predictable instants, anticipation improves performance. Knowledge of event timing modulates motor circuits and thereby improves response speed. By contrast, the neuronal mechanisms that underlie changes in sensory perception resulting from expectation are not well understood. We developed a behavioral procedure for rats in which we manipulated expectations about sound timing. Valid expectations improved both the speed and the accuracy of the subjects' performance, indicating not only improved motor preparedness but also enhanced perception. Single-neuron recordings in primary auditory cortex showed enhanced representation of sounds during periods of heightened expectation. Furthermore, we found that activity in auditory cortex was causally linked to the performance of the task and that changes in the neuronal representation of sounds predicted performance on a trial-by-trial basis. Our results indicate that changes in neuronal representation as early as primary sensory cortex mediate the perceptual advantage conferred by temporal expectation.     

Quantitative modeling of perception and production of time intervals.

The accurate perception/production of durations in the seconds and minutes range is important in a number of everyday activities, but the lack of direct experimental evidence on the neural circuits that could be involved has precluded the detailed elucidation of the underlying physiological mechanisms. We show, using a basic biophysical model of a timekeeping system and experimental data on time intervals produced or estimated under different conditions, that experimental values, variability, and distributions can be quantitatively explained in terms of a background synaptic activity such as that generated by attention. The model provides a plausible neural substrate for encoding time intervals, and the findings suggest how it may interplay at the single neuron level with the attentional system, to elaborate a subjective representation of the elapsing time.