Early Sensory Cortices Research Articles

Neuronal and Behavioral Responses to Naturalistic Texture Images in Macaque Monkeys.

The visual world is richly adorned with texture, which can serve to delineate important elements of natural scenes. In anesthetized macaque monkeys, selectivity for the statistical features of natural texture is weak in V1, but substantial in V2, suggesting that neuronal activity in V2 might directly support texture perception. To test this, we investigated the relation between single cell activity in macaque V1 and V2 and simultaneously measured behavioral judgments of texture. We generated stimuli along a continuum between naturalistic texture and phase-randomized noise and trained two macaque monkeys to judge whether a sample texture more closely resembled one or the other extreme. Analysis of responses revealed that individual V1 and V2 neurons carried much less information about texture naturalness than behavioral reports. However, the sensitivity of V2 neurons, especially those preferring naturalistic textures, was significantly closer to that of behavior compared with V1. The firing of both V1 and V2 neurons predicted perceptual choices in response to repeated presentations of the same ambiguous stimulus in one monkey, despite low individual neural sensitivity. However, neither population predicted choice in the second monkey. We conclude that neural responses supporting texture perception likely continue to develop downstream of V2. Further, combined with neural data recorded while the same two monkeys performed an orientation discrimination task, our results demonstrate that choice-correlated neural activity in early sensory cortex is unstable across observers and tasks, untethered from neuronal sensitivity, and therefore unlikely to directly reflect the formation of perceptual decisions.

Cortical Layer-Dependent Signaling in Cognition: Three Computational Modes of the Canonical Circuit.

The cerebral cortex performs computations via numerous six-layer modules. The operational dynamics of these modules were studied primarily in early sensory cortices using bottom-up computation for response selectivity as a model, which has been recently revolutionized by genetic approaches in mice. However, cognitive processes such as recall and imagery require top-down generative computation. The question of whether the layered module operates similarly in top-down generative processing as in bottom-up sensory processing has become testable by advances in the layer identification of recorded neurons in behaving monkeys. This review examines recent advances in laminar signaling in these two computations, using predictive coding computation as a common reference, and shows that each of these computations recruits distinct laminar circuits, particularly in layer 5, depending on the cognitive demands. These findings highlight many open questions, including how different interareal feedback pathways, originating from and terminating at different layers, convey distinct functional signals.

Perceptual Learning of Fine Contrast Discrimination Under Non-roving, Roving-Without-Flanker, and Roving-with-Flanker Conditions and its Relation to Neuronal Activity in Macaque V1

AbstractPerceptual learning refers to an improvement in perceptual abilities with training. Neural signatures of visual perceptual learning have been demonstrated mostly in mid- and high-level cortical areas, while changes in early sensory cortex were often more limited. We recorded continuously from multiple neuronal clusters in area V1 while macaque monkeys learned a fine contrast categorization task. Monkeys performed the contrast discrimination task initially when a constant-contrast sample stimulus was followed by a test stimulus of variable contrast, whereby they had to indicate whether the test was of lower or higher contrast than the sample. This was followed by sessions where we employed stimulus roving; i.e. the contrast of the sample stimulus varied from trial to trial. Finally, we trained animals, under ‘stimulus roving-with-flanker’ conditions, where the test stimuli to be discriminated were flanked by ‘flanking stimuli’. Perceptual discrimination abilities improved under non-roving conditions and under roving-with-flanker conditions as training progressed. Neuronal discrimination abilities improved with training mostly under non-roving conditions, but the effect was modest and limited to the most difficult contrast. Choice probabilities, quantifying how well neural activity is correlated with choice, equally increased with training during non-roving, but not during either of the roving conditions (with and without flankers). Noise correlations changed with training in both monkeys, but the changes were not consistent between monkeys. In one monkey, noise correlations decreased with training for non-roving and both roving conditions. In the other monkey, noise correlations changed for some conditions, but lacked a systematic pattern. Thus, while perceptual learning occurred under non-roving and roving-with-flanker conditions, the changes in neural activity in V1 were overall modest and were essentially absent under the different roving conditions.

Sleep-like changes in neural processing emerge during sleep deprivation in early auditory cortex.

Insufficient sleep is commonplace in modern lifestyle and can lead to grave outcomes, yet the changes in neuronal activity accumulating over hours of extended wakefulness remain poorly understood. Specifically, which aspects of cortical processing are affected by sleep deprivation (SD), and whether they also affect early sensory regions, remain unclear. Here, we recorded spiking activity in the rat auditory cortex along with polysomnography while presenting sounds during SD followed by recovery sleep. We found that frequency tuning, onset responses, and spontaneous firing rates were largely unaffected by SD. By contrast, SD decreased entrainment to rapid (≥20Hz) click trains, increased population synchrony, and increased the prevalence of sleep-like stimulus-induced silent periods, even when ongoing activity was similar. Recovery NREM sleep was associated with similar effects as SD with even greater magnitude, while auditory processing during REM sleep was similar to vigilant wakefulness. Our results show that processes akin to those in NREM sleep invade the activity of cortical circuits during SD, even in the early sensory cortex.

Visual perceptual load and processing of somatosensory stimuli in primary and secondary somatosensory cortices

Load theory assumes that neural activation to distractors in early sensory cortices is modulated by the perceptual load of a main task, regardless of whether task and distractor share the same sensory modality or not. While several studies have investigated the question of load effects on distractor processing in early sensory areas, there is no functional magnetic resonance imaging (fMRI) study regarding load effects on somatosensory stimuli. Here, we used fMRI to investigate effects of visual perceptual load on neural responses to somatosensory stimuli applied to the wrist in a study with 44 participants. Perceptual load was manipulated by an established sustained visual detection task, which avoided simultaneous target and distractor presentations. Load was operationalized by detection difficulty of subtle or clear color changes of one of 12 rotating dots. While all somatosensory stimuli led to activation in somatosensory areas SI and SII, we found no statistically significant difference in brain activation to these stimuli under high compared to low sustained visual load. Moreover, exploratory Bayesian analyses supported the absence of differences. Thus, our findings suggest a resistance of somatosensory processing to at least some forms of visual perceptual load, possibly due to behavioural relevance of discrete somatosensory stimuli and separable attentional resources for the somatosensory and visual modality.

Severely Attenuated Visual Feedback Processing in Children on the Autism Spectrum.

Individuals on the autism spectrum often exhibit atypicality in their sensory perception, but the neural underpinnings of these perceptual differences remain incompletely understood. One proposed mechanism is an imbalance in higher-order feedback re-entrant inputs to early sensory cortices during sensory perception, leading to increased propensity to focus on local object features over global context. We explored this theory by measuring visual evoked potentials during contour integration as considerable work has revealed that these processes are largely driven by feedback inputs from higher-order ventral visual stream regions. We tested the hypothesis that autistic individuals would have attenuated evoked responses to illusory contours compared with neurotypical controls. Electrophysiology was acquired while 29 autistic and 31 neurotypical children (7-17 years old, inclusive of both males and females) passively viewed a random series of Kanizsa figure stimuli, each consisting of four inducers that were aligned either at random rotational angles or such that contour integration would form an illusory square. Autistic children demonstrated attenuated automatic contour integration over lateral occipital regions relative to neurotypical controls. The data are discussed in terms of the role of predictive feedback processes on perception of global stimulus features and the notion that weakened "priors" may play a role in the visual processing anomalies seen in autism.SIGNIFICANCE STATEMENT Children on the autism spectrum differ from typically developing children in many aspects of their processing of sensory stimuli. One proposed mechanism for these differences is an imbalance in higher-order feedback to primary sensory regions, leading to an increased focus on local object features rather than global context. However, systematic investigation of these feedback mechanisms remains limited. Using EEG and a visual illusion paradigm that is highly dependent on intact feedback processing, we demonstrated significant disruptions to visual feedback processing in children with autism. This provides much needed experimental evidence that advances our understanding of the contribution of feedback processing to visual perception in autism spectrum disorder.

Neural correlates of emotional valence for faces and words.

Stimuli with negative emotional valence are especially apt to influence perception and action because of their crucial role in survival, a property that may not be precisely mirrored by positive emotional stimuli of equal intensity. The aim of this study was to identify the neural circuits differentially coding for positive and negative valence in the implicit processing of facial expressions and words, which are among the main ways human beings use to express emotions. Thirty-six healthy subjects took part in an event-related fMRI experiment. We used an implicit emotional processing task with the visual presentation of negative, positive, and neutral faces and words, as primary stimuli. Dynamic Causal Modeling (DCM) of the fMRI data was used to test effective brain connectivity within two different anatomo-functional models, for the processing of words and faces, respectively. In our models, the only areas showing a significant differential response to negative and positive valence across both face and word stimuli were early visual cortices, with faces eliciting stronger activations. For faces, DCM revealed that this effect was mediated by a facilitation of activity in the amygdala by positive faces and in the fusiform face area by negative faces; for words, the effect was mainly imputable to a facilitation of activity in the primary visual cortex by positive words. These findings support a role of early sensory cortices in discriminating the emotional valence of both faces and words, where the effect may be mediated chiefly by the subcortical/limbic visual route for faces, and rely more on the direct thalamic pathway to primary visual cortex for words.

Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task

Do sensory cortices process more than one sensory modality?To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). Forthis, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). Weanalyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.

Integrating Visual Information into the Auditory Cortex Promotes Sound Discrimination through Choice-Related Multisensory Integration.

An increasing number of studies have shown that cross-modal interaction can occur in early sensory cortices. Yet, how neurons in sensory cortices integrate multisensory cues in perceptual tasks and to what extent this influences behavior is largely unclear. To investigate, we examined visual modulation of auditory responses in the primary auditory cortex (A1) in a two-alternative forced-choice task. During the task, male rats were required to make a behavioral choice based on the pure tone frequency (low vs high) of the self-triggered stimulus to get a water reward. The result showed that the presence of a noninformative visual cue did not uniformly influence auditory response, with frequently enhancing just one of them. Closely correlated with behavioral choice, the visual cue mainly enhanced responsiveness to the auditory cue indicating a movement direction contralateral to A1 being recorded. Operating in this fashion provided A1 neurons a superior capability to discriminate sound during multisensory trials. Concomitantly, behavioral data and decoding analysis revealed that visual cue presence could speed the process of sound discrimination. We also observed this differential multisensory integration effect in well-trained rats when tested with passive stimulation and under anesthesia, albeit to a much lesser extent. We did not see this differentially integrative effect while recording in A1 in another similar group of rats performing a free-choice task. These data suggest that auditory cortex can engage in meaningful audiovisual processing, and perceptual learning can modify its multisensory integration mechanism to meet task requirements.SIGNIFICANCE STATEMENT In the natural environment, visual stimuli are frequently accompanied by auditory cues. Although multisensory integration has traditionally been seen as a feature of associational cortices, recent studies have shown that cross-modal inputs can also influence neuronal activity in primary sensory cortices. However, exactly how neurons in sensory cortices integrate multisensory cues to guide behavioral choice is still unclear. Here, we describe a novel model of multisensory integration used by A1 neurons to shape auditory representations when rats performed a cue-guided task. We found that a task-irrelevant visual cue could specifically enhance the response of neurons in sound guiding to the contralateral choice. This differentially integrative model facilitated sound discrimination and behavioral choice. This result indicates that task engagement can modulate multisensory integration.

Thalamocortical axons regulate neurogenesis and laminar fates in the early sensory cortex

Area-specific axonal projections from the mammalian thalamus shape unique cellular organization in target areas in the adult neocortex. How these axons control neurogenesis and early neuronal fate specification is poorly understood. By using mutant mice lacking the majority of thalamocortical axons, we show that these axons are required for the production and specification of the proper number of layer 4 neurons in primary sensory areas by the neonatal stage. Part of these area-specific roles is played by the thalamus-derived molecule, VGF. Our work reveals that extrinsic cues from sensory thalamic projections have an early role in the formation of cortical cytoarchitecture by enhancing the production and specification of layer 4 neurons.

Individual Optimal Attentional Strategy in Motor Learning Tasks Characterized by Steady-State Somatosensory and Visual Evoked Potentials.

Focus of attention is one of the most influential factors facilitating motor performance. Previous evidence supports that the external focus (EF) strategy, which directs attention to movement outcomes, is associated with better motor performance than the internal focus (IF) strategy, which directs attention to body movements. However, recent studies have reported that the EF strategy is not effective for some individuals. Furthermore, neuroimaging studies have demonstrated that the frontal and parietal areas characterize individual optimal attentional strategies for motor tasks. However, whether the sensory cortices are also functionally related to individual optimal attentional strategy remains unclear. Therefore, the present study examined whether an individual’s sensory processing ability would reflect the optimal attentional strategy. To address this point, we explored the relationship between responses in the early sensory cortex and individuals’ optimal attentional strategy by recording steady-state somatosensory evoked potentials (SSSEP) and steady-state visual evoked potentials (SSVEP). Twenty-six healthy young participants first performed a motor learning task with reaching movements under IF and EF conditions. Of the total sample, 12 individuals showed higher after-effects under the IF condition than the EF condition (IF-dominant group), whereas the remaining individuals showed the opposite trend (EF-dominant group). Subsequently, we measured SSSEP from bilateral primary somatosensory cortices while presenting vibrotactile stimuli and measured SSVEP from bilateral primary visual cortices while presenting checkerboard visual stimuli. The degree of increasing SSSEP response when the individuals in the IF-dominant group directed attention to vibrotactile stimuli was significantly more potent than those in the EF-dominant individuals. By contrast, the individuals in the EF-dominant group showed a significantly larger SSVEP increase while they directed attention to visual stimuli compared with the IF-dominant individuals. Furthermore, a significant correlation was observed such that individuals with more robust IF dominance showed more pronounced SSSEP attention modulation. These results suggest that the early sensory areas have crucial brain dynamics to characterize an individual’s optimal attentional strategy during motor tasks. The response characteristics may reflect the individual sensory processing ability, such as control of priority to the sensory inputs. Considering individual cognitive traits based on the suitable attentional strategy could enhance adaptability in motor tasks.

Non‐stimulated regions in early visual cortex encode the contents of conscious visual perception

Predictions shape our perception. The theory of predictive processing poses that our brains make sense of incoming sensory input by generating predictions, which are sent back from higher to lower levels of the processing hierarchy. These predictions are based on our internal model of the world and enable inferences about the hidden causes of the sensory input data. It has been proposed that conscious perception corresponds to the currently most probable internal model of the world. Accordingly, predictions influencing conscious perception should be fed back from higher to lower levels of the processing hierarchy. Here, we used functional magnetic resonance imaging and multivoxel pattern analysis to show that non‐stimulated regions of early visual areas contain information about the conscious perception of an ambiguous visual stimulus. These results indicate that early sensory cortices in the human brain receive predictive feedback signals that reflect the current contents of conscious perception.

Rhythmic sampling revisited: Experimental paradigms and neural mechanisms.

Sampling of information is thought to be an important aspect of explorative behaviour. Evidence for it has been gained in behavioural assessments of a variety of overt and covert cognitive domains, including sensation, attention, memory, eye movements and dexterity. A common aspect across many findings is that sampling tends to exhibit a rhythmicity at low frequencies (theta, 4-8 Hz; alpha, 9-12 Hz). Neurophysiological investigations in a wide range of species, including rodents, non-human primates and humans have demonstrated the presence of sampling related neural oscillations in a number of brain areas ranging from early sensory cortex, hippocampus to high-level cognitive areas. However, to assess whether rhythmic sampling represents a general aspect of exploratory behaviour one must critically evaluate the task parameters, and their potential link with neural oscillations. Here we focus on sampling during attentive vision to present an overview on the experimental conditions that are used to investigate rhythmic sampling and associated oscillatory brain activity in this domain. This review aims to (1) provide guidelines to efficiently quantify behavioural rhythms, (2) compare results from human and non-human primate studies and (3) argue that the underlying neural mechanisms of sampling can co-occur in both sensory and high-level areas.

Audiovisual Interactions Among Near-Threshold Oscillating Stimuli in the Far Periphery Are Phase-Dependent.

Recent studies have highlighted the possible contributions of direct connectivity between early sensory cortices to audiovisual integration. Anatomical connections between the early auditory and visual cortices are concentrated in visual sites representing the peripheral field of view. Here, we aimed to engage early sensory interactive pathways with simple, far-peripheral audiovisual stimuli (auditory noise and visual gratings). Using a modulation detection task in one modality performed at an 84% correct threshold level, we investigated multisensory interactions by simultaneously presenting weak stimuli from the other modality in which the temporal modulation was barely-detectable (at 55 and 65% correct detection performance). Furthermore, we manipulated the temporal congruence between the cross-sensory streams. We found evidence for an influence of barely-detectable visual stimuli on the response times for auditory stimuli, but not for the reverse effect. These visual-to-auditory influences only occurred for specific phase-differences (at onset) between the modulated audiovisual stimuli. We discuss our findings in the light of a possible role of direct interactions between early visual and auditory areas, along with contributions from the higher-order association cortex. In sum, our results extend the behavioral evidence of audio-visual processing to the far periphery, and suggest – within this specific experimental setting – an asymmetry between the auditory influence on visual processing and the visual influence on auditory processing.

Hemispheric asymmetries in visual mental imagery.

Visual mental imagery is the faculty whereby we can "visualize" objects that are not in our line of sight. Longstanding evidence dating back over thirty years has shown that unilateral brain lesions, especially in the left temporal lobe, can impair aspects of this ability. Yet, there is currently no attempt to identify analogies between these neuropsychological findings of hemispheric asymmetry and those from other neuroscientific approaches. Here, we present a critical review of the available literature on the hemispheric laterality of visual mental imagery, by looking at cross-method patterns of evidence in the domains of lesion neuropsychology, neuroimaging, and direct cortical stimulation. Results can be summarized under three main axes. First, frontoparietal networks in both hemispheres appear to be associated with visual mental imagery. Second, lateralization patterns emerge in the temporal lobes, with the left inferior temporal lobe being the most common finding in the literature for endogenously generated images, especially, but not exclusively, when orthographic material is used to ignite imagery. Third, an opposite pattern of hemispheric laterality emerges when visual mental images are induced by exogenous stimulation; direct cortical electrical stimulation tends to produce visual imagery experiences predominantly when applied to the right temporal lobe. These patterns of hemispheric asymmetry are difficult to reconcile with the dominant model of visual mental imagery, which emphasizes the implication of early sensory cortices. They suggest instead that visual mental imagery relies on large-scale brain networks, with a crucial participation of high-level visual regions in the temporal lobes.

Meta-analytic evidence of differential prefrontal and early sensory cortex activity during non-social sensory perception in autism

Meta-analytic evidence of differential prefrontal and early sensory cortex activity during non-social sensory perception in autism

Symbolic categorization of novel multisensory stimuli in the human brain

When primates (both human and non-human) learn to categorize simple visual or acoustic stimuli by means of non-verbal matching tasks, two types of changes occur in their brain: early sensory cortices increase the precision with which they encode sensory information, and parietal and lateral prefrontal cortices develop a categorical response to the stimuli. Contrary to non-human animals, however, our species mostly constructs categories using linguistic labels. Moreover, we naturally tend to define categories by means of multiple sensory features of the stimuli. Here we trained adult subjects to parse a novel audiovisual stimulus space into 4 orthogonal categories, by associating each category to a specific symbol. We then used multi-voxel pattern analysis (MVPA) to show that during a cross-format category repetition detection task three neural representational changes were detectable. First, visual and acoustic cortices increased both precision and selectivity to their preferred sensory feature, displaying increased sensory segregation. Second, a frontoparietal network developed a multisensory object-specific response. Third, the right hippocampus and, at least to some extent, the left angular gyrus, developed a shared representational code common to symbols and objects. In particular, the right hippocampus displayed the highest level of abstraction and generalization from a format to the other, and also predicted symbolic categorization performance outside the scanner. Taken together, these results indicate that when humans categorize multisensory objects by means of language the set of changes occurring in the brain only partially overlaps with that described by classical models of non-verbal unisensory categorization in primates.

Amplitude modulations of cortical sensory responses in pulsatile evidence accumulation.

How does the brain internally represent a sequence of sensory information that jointly drives a decision-making behavior? Studies of perceptual decision-making have often assumed that sensory cortices provide noisy but otherwise veridical sensory inputs to downstream processes that accumulate and drive decisions. However, sensory processing in even the earliest sensory cortices can be systematically modified by various external and internal contexts. We recorded from neuronal populations across posterior cortex as mice performed a navigational decision-making task based on accumulating randomly timed pulses of visual evidence. Even in V1, only a small fraction of active neurons had sensory-like responses time-locked to each pulse. Here, we focus on how these 'cue-locked' neurons exhibited a variety of amplitude modulations from sensory to cognitive, notably by choice and accumulated evidence. These task-related modulations affected a large fraction of cue-locked neurons across posterior cortex, suggesting that future models of behavior should account for such influences.

Modelling binocular disparity processing from statistics in natural scenes

The statistics of our environment impact not only our behavior, but also the selectivity and connectivity of the early sensory cortices. Over the last fifty years, powerful theories such as efficient coding, sparse coding, and the infomax principle have been proposed to explain the nature of this influence. Numerous computational and theoretical studies have since demonstrated solid, testable evidence in support of these theories, especially in the visual domain. However, most such work has concentrated on monocular, luminance-field descriptions of natural scenes, and studies that systematically focus on binocular processing of realistic visual input have only been conducted over the past two decades. In this review, we discuss the most recent of these binocular computational studies, with particular emphasis on disparity selectivity. We begin with a report of the relevant literature demonstrating concrete evidence for the relationship between natural disparity statistics, neural selectivity, and behavior. This is followed by a discussion of supervised and unsupervised computational studies. For each study, we include a description of the input data, theoretical principles employed in the models, and the contribution of the results in explaining biological data (neural and behavioral). In the discussion, we compare these models to the binocular energy model, and examine their application to the modelling of normal and abnormal development of vision. We conclude with a short description of what we believe are the most important limitations of the current state-of-the-art, and directions for future work which could address these shortcomings and enrich current and future models.

Visual Perception: Human Brain Cells Cause a Change of View

Some images spontaneously change in appearance. A new study has found that these changes are reflectedin high-level visual cortical areas before they become apparent in early sensory cortex. This suggests that visual information not only flows towards interpretative areas of our brain, but also in the reverse direction.