The role of feedback in shaping neural representations in cat visual cortex

Abstract

In the primary visual cortex, neurons with similar response preferences are grouped into domains forming continuous maps of stimulus orientation and direction of movement. These properties are widely believed to result from the combination of ascending and lateral interactions in the visual system. We have tested this view by examining the influence of deactivating feedback signals descending from the visuoparietal cortex on the emergence of these response properties and representations in cat area 18. We thermally deactivated the dominant motion-processing region of the visuoparietal cortex and used optical and electrophysiological methods to assay neural activity evoked in area 18 by stimulation with moving gratings and fields of coherently moving randomly distributed dots. Feedback deactivation decreased signal strength in both orientation and direction maps and virtually abolished the global layout of direction maps, whereas the basic structure of the orientation maps was preserved. These findings could be accounted for by a selective silencing of highly direction-selective neurons and by the redirection of preferences of less selective neurons. Our data suggest that signals fed back from the visuoparietal cortex strongly contribute to the emergence of direction selectivity in early visual areas. Thus we propose that higher cortical areas have significant influence over fundamental neuronal properties as they emerge in lower areas.

A neurochemical signature of visual recovery after extrastriate cortical damage in the adult cat

“…This effect was significantly more pronounced in area 18 than in areas 17 and 19 and affected calbindin-positive cells to a larger degree than parvalbumin-positive cells (Huxlin and Pasternak, 2004). This is consistent with electrophysiological studies, which show that when higher level visual cortical areas are temporarily inactivated, cortical neurons at earlier levels of the visual system exhibit a decrease in the amplitude of their responses to stimulation (Hupe et al, 1998;Wang et al, 2000;Galuske et al, 2002;Bardy et al, 2006). This suggests that the major influence of feedback projections on early visual neurons is excitatory in nature.…”

Selective interhemispheric circuits account for a cardinal bias in spontaneous activity within early visual areas

“…In agreement, stimulusderived maps in ferrets deteriorated only in vigor but not in layout when deactivating VICs (Schmidt et al, 2010). Also, feedback from the motionsensitive posterior-medial suprasylvian cortex did not instruct orientation but only direction preference maps (Galuske et al, 2002). This indicates that the feed forward loop and the intrahemispheric network provide sufficient structured input to maintain orientation maps close to the visual field's midline representation when callosal (or feedback) inputs are absent.…”

“…Thirdly, intrahemispheric feedback could contribute to spontaneous activity because it has considerable impact on stimulus-driven activity in area 18 (Wang et al, 2000;Galuske et al, 2002). However, anatomical studies indicate that feedback connections exhibit a lesser degree of orientation selectivity (Stettler et al, 2002) than intracortical axons and deactivation studies did not reveal pronounced specificity.…”

Precise Spatiotemporal Patterns among Visual Cortical Areas and Their Relation to Visual Stimulus Processing

“…These distributed activities must somehow be bound or combined together to create a coherent object segregated from the background. Suggested mechanisms of perceptual grouping and segmentation use both low-level and high-level cues (Palmer, 1992) and are supported by a rich network of feedforward, horizontal, and feedback connections (Rockland and Lund, 1982;Gilbert and Wiesel, 1989;Malach et al, 1993;Salin and Bullier, 1995;Hupé et al, 1998Hupé et al, , 2001Galuske et al, 2002;Stettler et al, 2002;Bullier, 2004;Shmuel et al, 2005).…”