Area V1 Research Articles

Orthogonalization of spontaneous and stimulus-driven activity by hierarchical neocortical areal network in primates

How biological neural networks reliably process information in the presence of spontaneous activity remains controversial. In mouse primary visual cortex (V1), stimulus-evoked and spontaneous activity show orthogonal (dissimilar) patterns, which is advantageous for separating sensory signals from internal noise. However, studies in carnivore and primate V1, which have functional columns, have reported high similarity between stimulus-evoked and spontaneous activity. Thus, the mechanism of signal-noise separation in the columnar visual cortex may be different from that in rodents. To address this issue, we compared spontaneous and stimulus-evoked activity in marmoset V1 and higher visual areas. In marmoset V1, spontaneous and stimulus-evoked activity showed similar patterns as expected. However, in marmoset higher visual areas, spontaneous and stimulus-evoked activity were progressively orthogonalized along the cortical hierarchy, eventually reaching levels comparable to those in mouse V1. These results suggest that orthogonalization of spontaneous and stimulus-evoked activity is a general principle of cortical computation.

Context-dependent orientation discontinuity encoding by gamma rhythms in mouse primary visual cortex.

Through the modulation of its surround, an identical visual stimulus can be perceived as more or less salient, allowing it to either stand out or seamlessly integrate with the rest of the visual scene. Gamma rhythms are associated with processing stimulus features across extensive areas of the visual field. Consistent with this concept, the magnitude of visually induced gamma rhythm depends on how well stimulus features aligned both within and outside the classical receptive field (CRF) at the recording site. However, there still exists some uncertainty regarding the encoding of context-modulated orientation discontinuity by gamma rhythms. To address this concern, we conducted extracellular recordings in layers II/III and IV of area V1 using lightly anaesthetized mice to investigate the gamma tuning for stimuli with orientation discontinuity. Our study revealed that gamma rhythms exhibit a preference for stimuli with orientation discontinuity similar to the spiking responses observed in V1, which contradicts the findings of previous studies. Furthermore, the gamma tuning of discontinuous orientations exhibits a moderate correlation with spike tuning and a positive correlation with the strength of surround suppression. Therefore, our study suggests a close association between gamma tuning and nearby spiking tuning; additionally, it highlights the connection between the encoding of visual features by gamma rhythms and functional architecture, as well as neural signal integration. KEY POINTS: Visual context modulates the gamma rhythms in the primary visual cortex. Discontinuous orientation elicits significantly enhanced gamma rhythms compared to the iso-orientation stimulus. The gamma tuning of discontinuous orientations exhibits a moderate correlation with spike tuning. Gamma tuning of orientation discontinuity exhibits a positive correlation with the strength of surround suppression.

High-density recording reveals sparse clusters (but not columns) for shape and texture encoding in macaque V4.

Macaque area V4 includes neurons that exhibit exquisite selectivity for visual form and surface texture, but their functional organization across laminae is unknown. We used high-density Neuropixels probes in two awake monkeys (one female and one male) to characterize shape and texture tuning of dozens of neurons simultaneously across layers. We found sporadic clusters of neurons that exhibit similar tuning for shape and texture: ∼20% exhibited similar tuning with their neighbors. Importantly, these clusters were confined to a few layers, seldom 'columnar' in structure. This was the case even when neurons were strongly driven, and exhibited robust contrast invariance for shape and texture tuning. We conclude that functional organization in area V4 is not columnar for shape and texture stimulus features and in general organization maybe at a coarser stimulus category scale (e.g. selectivity for stimuli with vs without 3D cues), and a coarser spatial scale (assessed by optical imaging), rather than at a fine scale in terms of similarity in single neuron tuning for specific features. We speculate that this may be a direct consequence of the great diversity of inputs integrated by V4 neurons to build variegated tuning manifolds in a high-dimensional space.Significance Statement In the primary visual cortex of the macaque monkey, studies have demonstrated columnar functional organization, i.e. shared tuning across layers for stimulus orientation, spatial frequency, ocular dominance, etc. In mid and higher level visual form processing stages, where neurons exhibit high-dimensional tuning, functional organization has been harder to evaluate. Here, leveraging the use of the high-density Neuropixels probes to record simultaneously from dozens of neurons across cortical layers, we demonstrate that functional organization is not columnar for shape and texture tuning in area V4, a midlevel stage critical for form processing. Our results contribute to the debate about the functional significance of cortical columns providing support to the idea that they emerge due to one-to-many representational expansion.

Brain state and cortical layer-specific mechanisms underlying perception at threshold

Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral outcomes despite similarities in sensory input. We sought to understand how fluctuations in behavioral state and cortical layer and cell class-specific neural activity underlie this perceptual variability. We analyzed physiological measurements of state and laminar electrophysiological activity in visual area V4 while monkeys were rewarded for correctly reporting a stimulus change at perceptual threshold. Hit trials were characterized by a behavioral state with heightened arousal, greater eye position stability, and enhanced decoding performance of stimulus identity from neural activity. Target stimuli evoked stronger responses in V4 in hit trials, and excitatory neurons in the superficial layers, the primary feed-forward output of the cortical column, exhibited lower variability. Feed-forward interlaminar population correlations were stronger on hits. Hit trials were further characterized by greater synchrony between the output layers of the cortex during spontaneous activity, while the stimulus-evoked period showed elevated synchrony in the feed-forward pathway. Taken together, these results suggest that a state of elevated arousal and stable retinal images allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.

Brain state and cortical layer-specific mechanisms underlying perception at threshold

Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral outcomes despite similarities in sensory input. We sought to understand how fluctuations in behavioral state and cortical layer and cell class-specific neural activity underlie this perceptual variability. We analyzed physiological measurements of state and laminar electrophysiological activity in visual area V4 while monkeys were rewarded for correctly reporting a stimulus change at perceptual threshold. Hit trials were characterized by a behavioral state with heightened arousal, greater eye position stability, and enhanced decoding performance of stimulus identity from neural activity. Target stimuli evoked stronger responses in V4 in hit trials, and excitatory neurons in the superficial layers, the primary feed-forward output of the cortical column, exhibited lower variability. Feed-forward interlaminar population correlations were stronger on hits. Hit trials were further characterized by greater synchrony between the output layers of the cortex during spontaneous activity, while the stimulus-evoked period showed elevated synchrony in the feed-forward pathway. Taken together, these results suggest that a state of elevated arousal and stable retinal images allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.

Dissociation of Attentional State and Behavioral Outcome Using Local Field Potentials.

Successful behavior depends on the attentional state and other factors related to decision-making, which may modulate neuronal activity differently. Here, we investigated whether attentional state and behavioral outcome (i.e., whether a target is detected or missed) are distinguishable using the power and phase of local field potential recorded bilaterally from area V4 of two male rhesus monkeys performing a cued visual attention task. To link each trial's outcome to pairwise measures of attention that are typically averaged across trials, we used several methods to obtain single-trial estimates of spike count correlation and phase consistency. Surprisingly, while attentional location was best discriminated using gamma and high-gamma power, behavioral outcome was best discriminated by alpha power and steady-state visually evoked potential. Power outperformed absolute phase in attentional/behavioral discriminability, although single-trial gamma phase consistency provided reasonably high attentional discriminability. Our results suggest a dissociation between the neuronal mechanisms that regulate attentional focus and behavioral outcome.

ViCo: Human visual perception-based contour extraction of Chinese Tang dynasty textile patterns

The study of ancient textile patterns not only enriches historical material but also inspires modern costume art design. Recent developments in computer vision technology provide novel analytical methods for the study of ancient textile patterns. As contours are one of the most significant features in computer vision tasks, contour extraction serves as a prerequisite to accomplishing intelligent understanding and automatic design of textile patterns. In this paper, a perception-consistent contour extraction method (ViCo) that simulates the human visual system from the retina, the lateral geniculate nucleus (LGN), to the V1 area in the cortex is proposed, along with an ancient textile pattern dataset represented by TuanKe in the Chinese Tang dynasty. Experiments were conducted both qualitatively and quantitatively to verify the effectiveness of the proposed method on the TuanKe dataset. Analysis of the results implies the effectiveness of ViCo because the retinal and LGN filter enhances edge information and restrains tiny pixel changes, and the cortex simulation is direction selective. This study is among the initial efforts to employ computer vision technology for ancient textile pattern studies. The study presents a TuanKe dataset and a novel bio-inspired contour extraction method, which has significant historical research importance, fabric art design inspiration, and computer application value.

The representational geometry for naturalistic textures in macaque V1 and V2.

Our understanding of visual cortical processing has relied primarily on studying the selectivity of individual neurons in different areas. A complementary approach is to study how the representational geometry of neuronal populations differs across areas. Though the geometry is derived from individual neuronal selectivity, it can reveal encoding strategies difficult to infer from single neuron responses. In addition, recent theoretical work has begun to relate distinct functional objectives to different representational geometries. To understand how the representational geometry changes across stages of processing, we measured neuronal population responses in primary visual cortex (V1) and area V2 of macaque monkeys to an ensemble of synthetic, naturalistic textures. Responses were lower dimensional in V2 than V1, and there was a better alignment of V2 population responses to different textures. The representational geometry in V2 afforded better discriminability between out-of-sample textures. We performed complementary analyses of standard convolutional network models, which did not replicate the representational geometry of cortex. We conclude that there is a shift in the representational geometry between V1 and V2, with the V2 representation exhibiting features of a low-dimensional, systematic encoding of different textures and of different instantiations of each texture. Our results suggest that comparisons of representational geometry can reveal important transformations that occur across successive stages of visual processing.

Local stimulation of pyramidal neurons in deep cortical layers of anesthetized rats enhances cortical visual information processing

In the primary visual cortex area V1 activation of inhibitory interneurons, which provide negative feedback for excitatory pyramidal neurons, can improve visual response reliability and orientation selectivity. Moreover, optogenetic activation of one class of interneurons, parvalbumin (PV) positive cells, reduces the receptive field (RF) width. These data suggest that in V1 the negative feedback improves visual information processing. However, according to information theory, noise can limit information content in a signal, and to the best of our knowledge, in V1 signal-to-noise ratio (SNR) has never been estimated following either pyramidal or inhibitory neuron activation. Therefore, we optogenetically activated pyramidal or PV neurons in the deep layers of cortical area V1 and measured the SNR and RF area in nearby pyramidal neurons. Activation of pyramidal or PV neurons increased the SNR by 267% and 318%, respectively, and reduced the RF area to 60.1% and 77.5%, respectively, of that of the control. A simple integrate-and-fire neuron model demonstrated that an improved SNR and a reduced RF area can increase the amount of information encoded by neurons. We conclude that in V1 activation of pyramidal neurons improves visual information processing since the location of the visual stimulus can be pinpointed more accurately (via a reduced RF area), and more information is encoded by neurons (due to increased SNR).

Contrast gain control is a reparameterization of a population response curve.

Neurons in primary visual cortex (area V1) adapt in varying degrees to the average contrast of the environment, suggesting that the representation of visual stimuli may interact with the state of cortical gain control in complex ways. To investigate this possibility, we measured and analyzed the responses of neural populations in mouse V1 to visual stimuli as a function of contrast in different environments, each characterized by a unique distribution of contrast values. Our findings reveal that, for a fixed stimulus, the population response can be described by a vector function r(gec), where the gain ge is a decreasing function of the mean contrast of the environment. Thus, gain control can be viewed as a reparameterization of a population response curve, which is invariant across environments. Different stimuli are mapped to distinct curves, all originating from a common origin, corresponding to a zero-contrast response. Altogether, our findings provide a straightforward, geometric interpretation of contrast gain control at the population level and show that changes in gain are well matched among members of a population.NEW & NOTEWORTHY The authors study the responses of neural populations in mouse primary visual cortex as a function of stimulus contrast. Measurements are performed in different "environments," each characterized by a different distribution of contrast values. They find that responses across environments can be viewed as a reparameterization of a single contrast-response curve, offering a simple, geometric account of contrast gain control in neural populations.

Attention Modulates Human Visual Responses to Objects by Tuning Sharpening.

Visual stimuli compete with each other for cortical processing and attention biases this competition in favor of the attended stimulus. How does the relationship between the stimuli affect the strength of this attentional bias? Here, we used functional MRI to explore the effect of target-distractor similarity in neural representation on attentional modulation in the human visual cortex using univariate and multivariate pattern analyses. Using stimuli from four object categories (human bodies, cats, cars and houses), we investigated attentional effects in the primary visual area V1, the object-selective regions LO and pFs, the body-selective region EBA, and the scene-selective region PPA. We demonstrated that the strength of the attentional bias towards the target is not fixed but decreases with increasing target-distractor similarity. Simulations provided evidence that this result pattern is explained by tuning sharpening rather than an increase in gain. Our findings provide a mechanistic explanation for behavioral effects of target-distractor similarity on attentional biases and suggest tuning sharpening as the underlying mechanism in object-based attention.

Recent Visual Experience Reshapes V4 Neuronal Activity and Improves Perceptual Performance.

Recent visual experience heavily influences our visual perception, but how neuronal activity is reshaped to alter and improve perceptual discrimination remains unknown. We recorded from populations of neurons in visual cortical area V4 while two male rhesus macaque monkeys performed a natural image change detection task under different experience conditions. We found that maximizing the recent experience with a particular image led to an improvement in the ability to detect a change in that image. This improvement was associated with decreased neural responses to the image, consistent with neuronal changes previously seen in studies of adaptation and expectation. We found that the magnitude of behavioral improvement was correlated with the magnitude of response suppression. Furthermore, this suppression of activity led to an increase in signal separation, providing evidence that a reduction in activity can improve stimulus encoding. Within populations of neurons, greater recent experience was associated with decreased trial-to-trial shared variability, indicating that a reduction in variability is a key means by which experience influences perception. Taken together, the results of our study contribute to an understanding of how recent visual experience can shape our perception and behavior through modulating activity patterns in the mid-level visual cortex.

Transcranial focused ultrasound modulates visual thalamus in a nonhuman primate model.

The thalamus plays a pivotal role as a neural hub, integrating and distributing visual information to cortical regions responsible for visual processing. Transcranial focused ultrasound (tFUS) has emerged as a promising non-invasive brain stimulation technology, enabling modulation of neural circuits with high spatial precision. This study investigates the tFUS neuromodulation at visual thalamus and characterizes the resultant effects on interconnected visual areas in a nonhuman primate model. Experiments were conducted on a rhesus macaque trained in a visual fixation task, combining tFUS stimulation with simultaneous scalp electroencephalography (EEG) and intracranial recordings from area V4, a region closely linked to the thalamus. Ultrasound was delivered through a 128-element random array ultrasound transducer operating at 700 kHz, with the focus steered onto the pulvinar of the thalamus based on neuroanatomical atlas and individual brain model. EEG source imaging revealed localized tFUS-induced activities in the thalamus, midbrain, and visual cortical regions. Critically, tFUS stimulation of the pulvinar can elicit robust neural responses in V4 without visual input, manifested as significant modulations in local field potentials, elevated alpha and gamma power, corroborating the functional thalamocortical connectivity. Furthermore, the tFUS neuromodulatory effects on visually-evoked V4 activities were region-specific within the thalamus and dependent on ultrasound pulse repetition frequency. This work provides direct electrophysiological evidence demonstrating the capability of tFUS in modulating the visual thalamus and its functional impact on interconnected cortical regions in a large mammalian model, paving the way for potential investigations for tFUS treating visual, sensory, and cognitive impairments.

Hue and orientation pinwheels in macaque area V4.

Area V4 is an intermediate-level area of the macaque visual cortical hierarchy that serves key functions in visual processing by integrating inputs from lower areas such as V1 and V2 and providing feedforward inputs to many higher cortical areas. Previous V4 imaging studies have focused on differential responses to color, orientation, disparity, and motion stimuli, but many details of the spatial organization of significant hue and orientation tuning have not been fully described. We used support vector machine (SVM) decoding of intrinsic cortical single-condition responses to generate high-resolution maps of hue and orientation tuning and to describe the organization of hue and orientation pinwheels in V4. Like V1 and V2, V4 contains maps of orientation that are organized as pinwheels. V4 also contains maps of hue that are organized as pinwheels, whose circular organization more closely represents the perception of hue than is observed in antecedent cortical areas. Unlike V1, where orientation is continuously mapped across the surface, V4 hue and orientation pinwheels are organized in limited numbers of pinwheel sequences. The organization of these sequences and the distance between pinwheels may provide insight into the functional organization of V4. Regions significantly tuned for hue occupy roughly four times that of the orientation, are largely separated from each other, and overlap by roughly 5%. This spatial organization is largely consistent with segregated inputs arising from V2 thin and interstripes. This modular organization of V4 suggests that further integration of color and shape might occur in higher areas in inferotemporal cortical.NEW & NOTEWORTHY The representation of hue and orientation in macaque monkey area V4 was determined by intrinsic cortical imaging of responses to isoluminant hues and achromatic grating stimuli. Vector summation of support vector machine (SVM) decoded single-condition responses was used to generate hue and orientation maps that, like V1 orientation maps, were both characterized by distinct pinwheel patterns. These data suggest that pinwheels are an important structure to represent different stimulus features across multiple visual cortical areas.

Brain Activation and Aberrant Effective Connectivity in the Mentalizing Network of Preadolescent Children at Familial High Risk of Schizophrenia or Bipolar Disorder

BackgroundSchizophrenia and bipolar disorder are characterized by social cognitive impairments, and recent research has identified alterations of the social brain. However, it is unknown whether familial high risk (FHR) of these disorders is associated with neurobiological alterations already present in childhood. MethodsAs part of the Danish High Risk and Resilience Study–VIA 11, we examined children at FHR of schizophrenia (n = 121, 50% female) or bipolar disorder (n = 75, 47% female) and population-based control children (PBCs) (n = 128, 48% female). Using functional magnetic resonance imaging and dynamic causal modeling, we investigated brain activation and effective connectivity during the social cognition paradigm from the Human Connectome Project. ResultsWe found similar activation of the mentalizing network across groups, including visual area V5, the dorsomedial prefrontal cortex, and the posterior superior temporal sulcus (pSTS). Nonetheless, both FHR groups showed aberrant brain connectivity in the form of increased feedforward connectivity from left V5 to pSTS compared with PBCs. Children at FHR of schizophrenia had reduced intrinsic connectivity in bilateral V5 compared with PBCs, whereas children at FHR of bipolar disorder showed increased reciprocal connectivity between the left dorsomedial prefrontal cortex and the pSTS, increased intrinsic connectivity in the right pSTS, and reduced feedforward connectivity from the right pSTS to the dorsomedial prefrontal cortex compared with PBCs. ConclusionsOur results provide first-time evidence of aberrant brain connectivity in the mentalizing network of children at FHR of schizophrenia or FHR of bipolar disorder. Longitudinal research is warranted to clarify whether aberrant brain connectivity during mentalizing constitutes an endophenotype associated with the development of a mental disorder later in life.

Contrast gain control is a reparameterization of a population response curve.

Neurons in primary visual cortex (area V1) adapt in different degrees to the average contrast of the environment, suggesting that the representation of visual stimuli may interact with the state of cortical gain control in complex ways. To investigate this possibility, we measured and analyzed the responses of neural populations to visual stimuli as a function of contrast in different environments, each characterized by a unique distribution of contrast. Our findings reveal that, for a given stimulus, the population response can be described by a vector function , where the gain is a decreasing function of the mean contrast of the environment. Thus, gain control can be viewed as a reparameterization of a population response curve, which is invariant across environments. Different stimuli are mapped to distinct curves, all originating from a common origin, corresponding to a zero-contrast response. Altogether, our findings provide a straightforward, geometric interpretation of contrast gain control at the population level and show that changes in gain are well coordinated among members of a neural population.

Human V4 size predicts crowding distance.

Visual recognition is limited by both object size (acuity) and spacing. The spacing limit, called "crowding", is the failure to recognize an object in the presence of other objects. Here, we take advantage of individual differences in crowding behavior to investigate its biological basis. Crowding distance, the minimum object spacing needed for recognition, varies 2-fold among healthy adults. We test the conjecture that this variation in psychophysical crowding distance is due to variation in cortical map size. To test this, we made paired measurements of brain and behavior in 50 observers. We used psychophysics to measure crowding distance and calculate λ, the number of letters that fit into each observer's visual field without crowding. In the same observers, we used fMRI to measure the surface area A (mm^2) of retinotopic maps V1, V2, V3, and V4. Across observers, λ is proportional to the surface area of V4 but is uncorrelated with the surface area of V1 to V3. The proportional relationship of λ to area of V4 indicates conservation of cortical crowding distance across individuals: letters can be recognized if they are spaced by at least 1.4 mm on the V4 map, irrespective of map size and psychophysical crowding distance. We conclude that the size of V4 predicts the spacing limit of visual perception.

The role of task on the human brain's responses to, and representation of, visual regularity defined by reflection and rotation

Identifying and segmenting objects in an image is generally achieved effortlessly and is facilitated by the presence of symmetry: a principle of perceptual organisation used to interpret sensory inputs from the retina into meaningful representations. However, while imaging studies show evidence of symmetry selective responses across extrastriate visual areas in the human brain, whether symmetry is processed automatically is still under debate. We used functional Magnetic Resonance Imaging (fMRI) to study the response to and representation of two types of symmetry: reflection and rotation. Dot pattern stimuli were presented to 15 human participants (10 female) under stimulus-relevant (symmetry) and stimulus-irrelevant (luminance) task conditions. Our results show that symmetry-selective responses emerge from area V3 and extend throughout extrastriate visual areas. This response is largely maintained when participants engage in the stimulus irrelevant task, suggesting an automaticity to processing visual symmetry. Our multi-voxel pattern analysis (MVPA) results extend these findings by suggesting that not only spatial organisation of responses to symmetrical patterns can be distinguished from that of non-symmetrical (random) patterns, but also that representation of reflection and rotation symmetry can be differentiated in extrastriate and object-selective visual areas. Moreover, task demands did not affect the neural representation of the symmetry information. Intriguingly, our MVPA results show an interesting dissociation: representation of luminance (stimulus irrelevant feature) is maintained in visual cortex only when task relevant, while information of the spatial configuration of the stimuli is available across task conditions. This speaks in favour of the automaticity for processing perceptual organisation: extrastriate visual areas compute and represent global, spatial properties irrespective of the task at hand.

Widespread receptive field remapping in early primate visual cortex

Predictive remapping of receptive fields (RFs) is thought to be one of the critical mechanisms for enforcing perceptual stability during eye movements. While RF remapping has been observed in several cortical areas, its role in early visual cortex and its consequences on the tuning properties of neurons have been poorly understood. Here, we track remapping RFs in hundreds of neurons from visual area V2 while subjects perform a cued saccade task. We find that remapping is widespread in area V2 across neurons from all recorded cortical layers and cell types. Furthermore, our results suggest that remapping RFs not only maintain but also transiently enhance their feature selectivity due to untuned suppression. Taken together, these findings shed light on the dynamics and prevalence of remapping in the early visual cortex, forcing us to revise current models of perceptual stability during saccadic eye movements.

Coordinated Response Modulations Enable Flexible Use of Visual Information.

We use sensory information in remarkably flexible ways. We can generalize by ignoring task-irrelevant features, report different features of a stimulus, and use different actions to report a perceptual judgment. These forms of flexible behavior are associated with small modulations of the responses of sensory neurons. While the existence of these response modulations is indisputable, efforts to understand their function have been largely relegated to theory, where they have been posited to change information coding or enable downstream neurons to read out different visual and cognitive information using flexible weights. Here, we tested these ideas using a rich, flexible behavioral paradigm, multi-neuron, multi-area recordings in primary visual cortex (V1) and mid-level visual area V4. We discovered that those response modulations in V4 (but not V1) contain the ingredients necessary to enable flexible behavior, but not via those previously hypothesized mechanisms. Instead, we demonstrated that these response modulations are precisely coordinated across the population such that downstream neurons have ready access to the correct information to flexibly guide behavior without making changes to information coding or synapses. Our results suggest a novel computational role for task-dependent response modulations: they enable flexible behavior by changing the information that gets out of a sensory area, not by changing information coding within it.