The Organization of Feedback Connections from Area V2 (18) to V1 (17)

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.

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Response Modulations by Static Texture Surround in Area V1 of the Macaque Monkey Do Not Depend on Feedback Connections From V2

Journal of Neurophysiology ◽

10.1152/jn.2001.85.1.146 ◽

2001 ◽

Vol 85 (1) ◽

pp. 146-163 ◽

Cited By ~ 89

Author(s):

Jean-Michel Hupé ◽

Andrew C. James ◽

Pascal Girard ◽

Jean Bullier

Keyword(s):

Visual Information ◽

Macaque Monkey ◽

V1 Neurons ◽

Orientation Contrast ◽

Area V2 ◽

Classical Receptive Field ◽

Main Effect ◽

Oriented Line ◽

Response Onset ◽

Feedback Connections

We analyzed the extracellular responses of 70 V1 neurons (recorded in 3 anesthetized macaque monkeys) to a single oriented line segment (or bar) placed within the cell classical receptive field (RF), or center of the RF. These responses could be modulated when rings of bars were placed entirely outside, but around the RF (the “near” surround region), as described in previous studies. Suppression was the main effect. The response was enhanced for 12 neurons when orthogonal bars in the surround were presented instead of bars having the same orientation as the center bar. This orientation contrast property is possibly involved in the mediation of perceptual pop-out. The enhancement was delayed compared with the onset of the response by about 40 ms. We also observed a suppression originating specifically from the flanks of the surround. This “side-inhibition,” significant for nine neurons, was delayed by about 20 ms. We tested whether these center/surround interactions in V1 depend on feedback connections from area V2. V2 was inactivated by GABA injections. We used devices made of six micropipettes to inactivate the convergent zone from V2 to V1. We could reliably inactivate a 2- to 4-mm-wide region of V2. Inactivation of V2 had no effect on the center/surround interactions of V1 neurons, even those that were delayed. Therefore the center/surround interactions of V1 neurons that might be involved in pop-out do not appear to depend on feedback connections from V2, at least in the anesthetized monkey. We conclude that these properties are probably shaped by long-range connections within V1 or depend on other feedback connections. The main effect of V2 inactivation was a decrease of the response to the single bar for about 10% of V1 neurons. The decrease was delayed by <20 ms after the response onset. Even the earliest neurons to respond could be affected by the feedback from V2. Together with the results on feedback connections from MT (previous paper), these findings show that feedback connections potentiate the responses to stimulation of the RF center and are recruited very early for the treatment of visual information.

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Faculty Opinions recommendation of A spatially organized representation of colour in macaque cortical area V2.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1011818.182621 ◽

2003 ◽

Author(s):

Kathleen Cullen

Keyword(s):

Cortical Area ◽

Area V2

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Myelin densities in retinotopically defined dorsal visual areas of the macaque

Brain Structure and Function ◽

10.1007/s00429-021-02363-z ◽

2021 ◽

Author(s):

Xiaolian Li ◽

Qi Zhu ◽

Wim Vanduffel

Keyword(s):

Visual Cortex ◽

Visual Field ◽

Cortical Thickness ◽

New World Monkeys ◽

Isotropic Resolution ◽

Density Mapping ◽

Area V2 ◽

Visual Areas ◽

Density Results

AbstractThe 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.

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

Nature Communications ◽

10.1038/s41467-021-24928-6 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Caitlin Siu ◽

Justin Balsor ◽

Sam Merlin ◽

Frederick Federer ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Projection Neurons ◽

V1 Neurons ◽

Cortical Areas ◽

Area V2 ◽

Computational Work ◽

Primate Visual Cortex ◽

Similar Area ◽

Hierarchical Computation

AbstractThe 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.

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Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus

Journal of Neurophysiology ◽

10.1152/jn.00757.2019 ◽

2020 ◽

Vol 124 (2) ◽

pp. 404-417 ◽

Cited By ~ 1

Author(s):

Peter W. Campbell ◽

Gubbi Govindaiah ◽

Sean P. Masterson ◽

Martha E. Bickford ◽

William Guido

Keyword(s):

Lateral Geniculate Nucleus ◽

Dorsal Lateral Geniculate Nucleus ◽

Thalamic Reticular Nucleus ◽

Reticular Nucleus ◽

Lateral Geniculate ◽

Dependent Form ◽

Dorsal Lateral Geniculate ◽

Feedback Connections ◽

Spike Firing ◽

Stimulation Of

The thalamic reticular nucleus (TRN) modulates thalamocortical transmission through inhibition. In mouse, TRN terminals in the dorsal lateral geniculate nucleus (dLGN) form synapses with relay neurons but not interneurons. Stimulation of TRN terminals in dLGN leads to a frequency-dependent form of inhibition, with higher rates of stimulation leading to a greater suppression of spike firing. Thus, TRN inhibition appears more dynamic than previously recognized, having a graded rather than an all-or-none impact on thalamocortical transmission.

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Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque

Experimental Brain Research ◽

10.1007/s00221-003-1698-8 ◽

2004 ◽

Vol 155 (1) ◽

pp. 102-110 ◽

Cited By ~ 9

Author(s):

Hiroyuki Nakamura ◽

Wu Ri Le ◽

Masumi Wakita ◽

Akichika Mikami ◽

Kazuo Itoh

Keyword(s):

Cytochrome Oxidase ◽

Visual Area ◽

Area V2 ◽

Posterior Area

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Border Ownership from Intracortical Interactions in Visual Area V2

Neuron ◽

10.1016/j.neuron.2005.04.005 ◽

2005 ◽

Vol 47 (1) ◽

pp. 143-153 ◽

Cited By ~ 85

Author(s):

Li Zhaoping

Keyword(s):

Visual Area ◽

Area V2

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Temporal Dynamics of Shape Analysis in Macaque Visual Area V2

Journal of Neurophysiology ◽

10.1152/jn.00822.2003 ◽

2004 ◽

Vol 92 (5) ◽

pp. 3030-3042 ◽

Cited By ~ 47

Author(s):

Jay Hegdé ◽

David C. Van Essen

Keyword(s):

Cortical Neurons ◽

Time Course ◽

Temporal Dynamics ◽

Visual Stimulation ◽

Signal To Noise Ratio ◽

Stimulus Onset ◽

Visual Area ◽

Response Modulation ◽

Population Response ◽

Area V2

The firing rate of visual cortical neurons typically changes substantially during a sustained visual stimulus. To assess whether, and to what extent, the information about shape conveyed by neurons in visual area V2 changes over the course of the response, we recorded the responses of V2 neurons in awake, fixating monkeys while presenting a diverse set of static shape stimuli within the classical receptive field. We analyzed the time course of various measures of responsiveness and stimulus-related response modulation at the level of individual cells and of the population. For a majority of V2 cells, the response modulation was maximal during the initial transient response (40–80 ms after stimulus onset). During the same period, the population response was relatively correlated, in that V2 cells tended to respond similarly to specific subsets of stimuli. Over the ensuing 80–100 ms, the signal-to-noise ratio of individual cells generally declined, but to a lesser degree than the evoked-response rate during the corresponding time bins, and the response profiles became decorrelated for many individual cells. Concomitantly, the population response became substantially decorrelated. Our results indicate that the information about stimulus shape evolves dynamically and relatively rapidly in V2 during static visual stimulation in ways that may contribute to form discrimination.

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