Visual input statistics and behavioral relevance jointly constrain higher visual cortex organization

Functional Specialization of Seven Mouse Visual Cortical Areas

Plasticity and Stability of the Visual System in Human Achiasma

Visual areas I and II of cerebral cortex of rabbit.

Ritchie et al. (this issue) argue that a deeper understanding of occipitotemporal cortex (OTC) requires shifting emphasis from category selectivity to behavioral relevance. They suggest that focusing on categories such as faces, bodies, or scenes is too narrow and overlooks how OTC supports flexible, goal-directed behavior. We agree that linking neural representations to behavior is essential but caution against treating category selectivity and behavioral relevance as opposing views. Category selectivity provides valuable insight into how cortical representations are organized to support behavior, and recent advances in computational modeling, particularly with deep neural networks, offer a powerful framework for probing this relationship.

For studies of visual cortex organization, mouse is becoming an increasingly more often used model. In addition to its genetic tractability, the relatively small area of cortical surface devoted to visual processing simplifies efforts in relating the structure of visual cortex to visual function. However, the nature of this compact organization can make some comparisons to the much larger non-human primate visual cortex difficult. The squirrel, as a highly visual rodent offers a useful means for better understanding how mouse and monkey cortical organization compares. More in line with primates than their nocturnal rodent cousin, squirrels rely much more on sight and have evolved a larger expanse of cortex devoted to visual processing. To reveal the detailed organization of visual cortex in squirrels, we injected a highly sensitive monosynaptic retrograde tracer (glycoprotein deleted rabies virus) into several locations of primary visual cortex (V1) in California ground squirrels. The resulting pattern of connectivity revealed an organizational scheme in the squirrel that retains some of the basic features of the mouse visual cortex along the medial and posterior borders of V1, but unlike mouse has an elaborate and extensive pattern laterally that is more similar to the early visual cortex organization found in monkeys. In this way, we show that the squirrel can serve as a useful model for comparison to both mouse and primate visual systems, and may help facilitate comparisons between these two very different yet widely used animal models of visual processing.

PROJECTION OF THE RETINA ON TO STRIATE AND PRESTRIATE CORTEX IN THE SQUIRREL MONKEY, SAIMIRI SCIUREUS.

Mid-level visual features directly support an array of behaviors; thus, they may be critical for understanding the functional organization of visual cortex. However, attempts at characterizing mid-level features have been hampered by the difficulty of describing these features in words—they exist in an “ineffable valley” between the describable patterns of low-level vision (e.g., edges) and the commonsense concepts of visual cognition (e.g., objects). Here we developed a novel approach to identify interpretable emergent properties of mid-level representations in deep neural network (DNN) models of visual cortex. Using this approach, we examined DNN models that were fit to scene-evoked fMRI responses in category-selective regions of visual cortex—specifically, scene-selective cortex (sceneDNN) and object-selective cortex (objectDNN). Our method uses a semantically-guided image-occlusion procedure to systematically characterize how DNN activations are driven by the classes of objects within a scene. We examined the relationship between mid-level features and several object properties that have previously been associated with response preferences in visual cortex: curvature, real-world size, animacy, naturalness, and spatial stability. We found that while mid-level features appear complex and difficult to describe at a surface level, large-scale computational analyses can reveal a latent underlying relationship to interpretable object properties. Specifically, we found that the mid-level representations of the sceneDNN support a latent preference for objects that are boxy and large in real-world size. In contrast, mid-level representations of the objectDNN support a complementary preference for objects that are curvy and small in real-world size. These effects were robust to variations of model hyperparameters and were reproducible across different DNN models. Our findings show that curvature and real-world size are emergent organizing principles of mid-level visual representation, and they suggest that differences in mid-level feature tuning may be critical for understanding the organization of visual cortex into category-selective patches.

In this study, we have investigated the organization of mouse visual cortex by correlating in detail the distribution of striate-extrastriate projections with the pattern of callosal connections revealed by the transport of horseradish peroxidase from the contralateral hemisphere. Single injections of 3H-proline into striate cortex produce 8-9 discrete projection fields in the belt of cortex surrounding area 17. The number and arrangement of these fields closely resemble the pattern of extrastriate visual areas in the rat. The callosal pattern is also very similar to that in the rat, and provides a set of landmarks for the location of the striate-recipient zones. Thus, cortical regions containing dense aggregations of callosal cells and terminations surround totally or partially the sparsely callosal striate-recipient zones. By comparing our results with previous accounts of the rat visual plan, we were able to identify in lateral extrastriate cortex of the mouse areas anterolateral (AL), lateromedial (LM), laterointermediate (LI), laterolateral (LL), posterolateral (PL), and posterior (P). We also observed 1-2 projections fields into anteromedial (AM) extrastriate cortex, and one field (S) into the posteromedial border of the head representation in primary somatosensory cortex. Our results support the notions that the visual cortex in the mouse is subdivided into multiple visual areas, and that these areas are arranged according to a plan that is common in rodents.

Numerous studies in visually deprived nonhuman animals have demonstrated sensitive periods for the functional development of the early visual cortex. However, in humans it is yet unknown which visual areas are shaped to which degree based on visual experience. The present study investigated the functional organization and processing capacities of early visual cortex in sight recovery individuals with either a history of congenital cataracts (CC) or late onset cataracts (developmental cataracts, DC). Visual event-related potentials (VERPs) were recorded to grating stimuli which were flashed in one of the four quadrants of the visual field. Participants had to detect rarely occurring grating orientations. The CC individuals showed the expected polarity reversal of the C1 wave between upper and lower visual field stimuli at the typical latency range. Since the C1 has been proposed to originate in the early retinotopic visual cortex, we concluded that one basic feature of the retinotopic organization, upper versus lower visual field organization, is spared in CC individuals. Group differences in the size and topography of the C1 effect, however, suggested a less precise functional tuning. The P1 wave, which has been associated with extrastriate visual cortex processing, was significantly attenuated in CC but not in DC individuals compared to typically sighted controls. The present study thus provides evidence for fundamental aspects of retinotopic processing in humans being independent of developmental vision. We suggest that visual impairments in sight recovery individuals may predominantly arise at higher cortical processing stages.

A hallmark of high-level visual cortex is its functional organization of neighboring areas that are selective for single categories, such as faces, bodies, and objects. However, visual scenes are typically composed of multiple categories. How does a category-selective cortex represent such complex stimuli? Previous studies have shown that the representation of multiple stimuli can be explained by a normalization mechanism. Here we propose that a normalization mechanism that operates in a cortical region composed of neighboring category-selective areas would generate a representation of multi-category stimuli that varies continuously across a category-selective cortex as a function of the magnitude of category selectivity for its components. By using fMRI, we can examine this correspondence between category selectivity and the representation of multi-category stimuli along a large, continuous region of cortex. To test these predictions, we used a linear model to fit the fMRI response of human participants (both sexes) to a multi-category stimulus (e.g., a whole person) based on the response to its component stimuli presented in isolation (e.g., a face or a body). Consistent with our predictions, the response of cortical areas in high-level visual cortex to multi-category stimuli varies in a continuous manner along a weighted mean line, as a function of the magnitude of its category selectivity. This was the case for both related (face + body) and unrelated (face+wardrobe) multi-category pairs. We conclude that the functional organization of neighboring category-selective areas may enable a dynamic and flexible representation of complex visual scenes that can be modulated by higher-level cognitive systems according to task demands.SIGNIFICANCE STATEMENT It is well established that the high-level visual cortex is composed of category-selective areas that reside in nearby locations. Here we predicted that this functional organization together with a normalization mechanism would generate a representation for multi-category stimuli that varies as a function of the category selectivity for its components. Consistent with this prediction, in an fMRI study we found that the representation of multi-category stimuli varies along high-level visual cortex, in a continuous manner, along a weighted mean line, in accordance with the category selectivity for a given area. These findings suggest that the functional organization of high-level visual cortex enables a flexible representation of complex scenes that can be modulated by high-level cognitive systems according to task demands.

Slow lorises (Nycticebus coucang) are nocturnal prosimian (i.e. strepsirhine) primates, closely related to bushbabies (Galago spp.). We examined the organization of visual cortex in four hemispheres from two slow lorises, using connectional and architectonic techniques. All hemispheres were flattened and sections stained for myelin and cytochrome oxidase (CO). Our results indicate, first, that the primary visual area (V1) in slow lorises has a system of small CO-dense blobs, as has been described in most other anthropoid and prosimian primates examined to date. The second visual area (V2) is characterized by broad, stripe-like zones of dense CO staining separated by zones of lighter staining. Loris V2 stripes are less distinct than those of anthropoid primates, and separate classes of thin and thick dark stripes are not apparent. However, V2 stripes are much better developed than in Galago, where they are virtually absent. Injections of wheat-germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) in area V1 revealed reciprocal connections with area V2, and the middle temporal (MT) and dorsolateral (DL) extrastriate areas. Area MT was also identified by its distinctive, dense myelination. As has been reported in anthropoids, DL can be divided into separate caudal and rostral divisions, which differ in myelin and CO staining, and in the strength of their connections with V1. Taken together, our results suggest that many of the features that characterize visual cortex organization in anthropoid primates are present in prosimians and thus probably evolved early in primate history, prior to the diversification of modern primate groups.

RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT.

Functional Organization of the Primary Visual Cortex

Elaborate organization of visual cortex in the hamster

The brain is capable of large-scale reorganization in blindness or after massive injury. Such reorganization crosses the division into separate sensory cortices (visual, somatosensory...). As its result, the visual cortex of the blind becomes active during tactile Braille reading. Although the possibility of such reorganization in the normal, adult brain has been raised, definitive evidence has been lacking. Here, we demonstrate such extensive reorganization in normal, sighted adults who learned Braille while their brain activity was investigated with fMRI and transcranial magnetic stimulation (TMS). Subjects showed enhanced activity for tactile reading in the visual cortex, including the visual word form area (VWFA) that was modulated by their Braille reading speed and strengthened resting-state connectivity between visual and somatosensory cortices. Moreover, TMS disruption of VWFA activity decreased their tactile reading accuracy. Our results indicate that large-scale reorganization is a viable mechanism recruited when learning complex skills.DOI: http://dx.doi.org/10.7554/eLife.10762.001