Cortical Circuits for Top-down Control of Perceptual Grouping

A fundamental characteristic of human visual perception is the ability to group together disparate elements in a scene and treat them as a single unit. The mechanisms by which humans create such groupings remain unknown, but grouping seems to play an important role in a wide variety of visual phenomena, and a good understanding of these mechanisms might provide guidance for how to improve machine vision algorithms. Here, we build on a proposal that some groupings are the result of connections in cortical area V2 that join disparate elements, thereby allowing them to be selected and segmented together. In previous instantiations of this proposal, connection formation was based on the anatomy (e.g., extent) of receptive fields, which made connection formation obligatory when the stimulus conditions stimulate the corresponding receptive fields. We now propose dynamic circuits that provide greater flexibility in the formation of connections and that allow for top-down control of perceptual grouping. With computer simulations we explain how the circuits work and show how they can account for a wide variety of Gestalt principles of perceptual grouping and two texture segmentation tasks. We propose that human observers use such top-down control to implement task-dependent connection strategies that encourage particular groupings of stimulus elements in order to promote performance on various kinds of visual tasks.

Myelin densities in retinotopically defined dorsal visual areas of the macaque

The visuotopic organization of dorsal visual cortex rostral to area V2 in primates has been a longstanding source of controversy. Using sub-millimeter phase-encoded retinotopic fMRI mapping, we recently provided evidence for a surprisingly similar visuotopic organization in dorsal visual cortex of macaques compared to previously published maps in New world monkeys (Zhu and Vanduffel, Proc Natl Acad Sci USA 116:2306–2311, 2019). Although individual quadrant representations could be robustly delineated in that study, their grouping into hemifield representations remains a major challenge. Here, we combined in-vivo high-resolution myelin density mapping based on MR imaging (400 µm isotropic resolution) with fine-grained retinotopic fMRI to quantitatively compare myelin densities across retinotopically defined visual areas in macaques. Complementing previously documented differences in populational receptive-field (pRF) size and visual field signs, myelin densities of both quadrants of the dorsolateral posterior area (DLP) and area V3A are significantly different compared to dorsal and ventral area V3. Moreover, no differences in myelin density were observed between the two matching quadrants belonging to areas DLP, V3A, V1, V2 and V4, respectively. This was not the case, however, for the dorsal and ventral quadrants of area V3, which showed significant differences in MR-defined myelin densities, corroborating evidence of previous myelin staining studies. Interestingly, the pRF sizes and visual field signs of both quadrant representations in V3 are not different. Although myelin density correlates with curvature and anticorrelates with cortical thickness when measured across the entire cortex, exactly as in humans, the myelin density results in the visual areas cannot be explained by variability in cortical thickness and curvature between these areas. The present myelin density results largely support our previous model to group the two quadrants of DLP and V3A, rather than grouping DLP- with V3v into a single area VLP, or V3d with V3A+ into DM.

A direct interareal feedback-to-feedforward circuit in primate visual cortex

The mammalian sensory neocortex consists of hierarchically organized areas reciprocally connected via feedforward (FF) and feedback (FB) circuits. Several theories of hierarchical computation ascribe the bulk of the computational work of the cortex to looped FF-FB circuits between pairs of cortical areas. However, whether such corticocortical loops exist remains unclear. In higher mammals, individual FF-projection neurons send afferents almost exclusively to a single higher-level area. However, it is unclear whether FB-projection neurons show similar area-specificity, and whether they influence FF-projection neurons directly or indirectly. Using viral-mediated monosynaptic circuit tracing in macaque primary visual cortex (V1), we show that V1 neurons sending FF projections to area V2 receive monosynaptic FB inputs from V2, but not other V1-projecting areas. We also find monosynaptic FB-to-FB neuron contacts as a second motif of FB connectivity. Our results support the existence of FF-FB loops in primate cortex, and suggest that FB can rapidly and selectively influence the activity of incoming FF signals.

Multimodal Neuroimaging Study of Visual Plasticity in Schizophrenia

Schizophrenia is a severe mental illness with visual learning and memory deficits, and reduced long term potentiation (LTP) may underlie these impairments. Recent human fMRI and EEG studies have assessed visual plasticity that was induced with high frequency visual stimulation, which is thought to mimic an LTP-like phenomenon. This study investigated the differences in visual plasticity in participants with schizophrenia and healthy controls. An fMRI visual plasticity paradigm was implemented, and proton magnetic resonance spectroscopy data were acquired to determine whether baseline resting levels of glutamatergic and GABA metabolites were related to visual plasticity response. Adults with schizophrenia did not demonstrate visual plasticity after family-wise error correction; whereas, the healthy control group did. There was a significant regional difference in visual plasticity in the left visual cortical area V2 when assessing group differences, and baseline GABA levels were associated with this specific ROI in the SZ group only. Overall, this study suggests that visual plasticity is altered in schizophrenia and related to basal GABA levels.

Processing of motion boundary orientation in macaque V2

Human and nonhuman primates are good at identifying an object based on its motion, a task that is believed to be carried out by the ventral visual pathway. However, the neural mechanisms underlying such ability remains unclear. We trained macaque monkeys to do orientation discrimination for motion boundaries (MBs) and recorded neuronal response in area V2 with microelectrode arrays. We found 10.9% of V2 neurons exhibited robust orientation selectivity to MBs, and their responses correlated with monkeys’ orientation-discrimination performances. Furthermore, the responses of V2 direction-selective neurons recorded at the same time showed correlated activity with MB neurons for particular MB stimuli, suggesting that these motion-sensitive neurons made specific functional contributions to MB discrimination tasks. Our findings support the view that V2 plays a critical role in MB analysis and may achieve this through a neural circuit within area V2.

Functional-Specific Projections from V2 to V4 in Macaque Monkeys

Previous studies have revealed modular projections from area V2 to area V4 in macaques. Specifically, V2 neurons in cytochrome oxidase (CO)-rich thin and CO-sparse pale stripes project to distinct regions in V4. However, how these modular projections relate to the functional subcompartments of V4 remains unclear. In this study, we injected retrograde fluorescent tracers into different functional domains (color, orientation, and direction) in V4 that were identified with intrinsic signal optical imaging. We examined the labeled neurons in area V2 and their locations with respect to the CO patterns. Covariation was observed between the functional properties of the V4 injection sites and the numbers of labeled neurons in particular CO stripes. This covariation indicates that the color domains in V4 mainly received inputs from V2 thin stripes, whereas V4 orientation domains received inputs from pale (major) and thick (minor) stripes. Although there are motion-sensitive domains in both V2 and V4, our results did not reveal a functional-specific feedforward projection between them. These results confirmed previous findings of modular projections from V2 to V4 and provided functional specificity for these anatomical projections. Together, these findings indicate that color and form remain separate in the ventral midlevel visual processing.

A sinusoidal transform of the visual field in cortical area V2

The retinotopic maps of many visual cortical areas are thought to follow the fundamental principles that have been described for primary visual cortex (V1) where nearby points on the retina map to nearby points on the surface of V1, and orthogonal axes of the retinal surface are represented along orthogonal axes of the cortical surface. Here we demonstrate a striking departure from this conventional mapping in the secondary visual area (V2) of the tree shrew. Although local retinotopy is preserved, orthogonal axes of the retina are represented along the same axis of the cortical surface, an unexpected geometry explained by an orderly sinusoidal transform of the retinal surface. This sinusoidal topography is ideally suited for achieving uniform coverage in an elongated area like V2, is predicted by mathematical models designed to achieve wiring minimization, and provides a novel explanation for stripe-like patterns of intra-cortical connections and stimulus response properties in V2. Our findings suggest that cortical circuits flexibly implement solutions to sensory surface representation, with dramatic consequences for the large-scale layout of topographic maps.

Stream-Specific Feedback Inputs to the Primate Primary Visual Cortex

ABSTRACTThe sensory neocortex consists of hierarchically-organized areas reciprocally connected via feedforward and feedback circuits. Feedforward connections shape the receptive field properties of neurons in higher areas within parallel streams specialized in processing specific stimulus attributes. Feedback connections, instead, have been implicated in top-down modulations, such as attention, prediction and sensory context. However, their computational role remains unknown, partly because we lack knowledge about rules of feedback connectivity to constrain models of feedback function. For example, it is unknown whether feedback connections maintain stream-specific segregation, or integrate information across parallel streams. Using selective viral-mediated labeling of feedback connections arising from specific cytochrome-oxidase stripes of macaque visual area V2, we find that feedback to the primary visual cortex (V1) is organized into parallel streams resembling the reciprocal feedforward pathways. These results suggest that functionally-specialized V2 feedback channels modulate V1 responses to specific stimulus attributes, an organizational principle that could extend to feedback pathways in other sensory systems.