Top-down feedback controls spatial summation and response amplitude in primate visual cortex

Abstract

Sensory information travels along feedforward connections through a hierarchy of cortical areas, which, in turn, send feedback connections to lower-order areas. Feedback has been implicated in attention, expectation, and sensory context, but the mechanisms underlying these diverse feedback functions are unknown. Using specific optogenetic inactivation of feedback connections from the secondary visual area (V2), we show how feedback affects neural responses in the primate primary visual cortex (V1). Reducing feedback activity increases V1 cells’ receptive field (RF) size, decreases their responses to stimuli confined to the RF, and increases their responses to stimuli extending into the proximal surround, therefore reducing surround suppression. Moreover, stronger reduction of V2 feedback activity leads to progressive increase in RF size and decrease in response amplitude, an effect predicted by a recurrent network model. Our results indicate that feedback modulates RF size, surround suppression and response amplitude, similar to the modulatory effects of visual spatial attention.

Cortico-cortical feedback from V2 exerts a powerful influence over the visually evoked local field potential and associated spike timing in V1

“…Recall that we used large (˜5°diameter) gratings that invaded the suppressive surrounds of V1 neurons. The increase in spike rate during cooling is therefore consistent with previous reports that feedback inactivation reduces surround suppression (Nassi et al, 2013(Nassi et al, , 2014Nurminen et al, 2018). Despite this increase in spike rate, the periodicity in spiking decreased across the vast majority of sites, whether measured as a change in gamma power (Fig.…”

“…Related to this second possibility and to previous findings that the peak frequency of gamma rhythms are modulated by stimulus size (Gieselmann and Thiele, 2008;Henrie and Shapley, 2005;Ray and Maunsell, 2010), we note two similarities between the effects of inactivating feedback to V1 in the monkey and local inactivation of somatostatinexpressing inhibitory interneurons (SOMs) in V1 of mice. In monkeys, V2/V3 inactivation produced a reduction in surround suppression in V1 (Nassi et al, 2013(Nassi et al, , 2014Nurminen et al, 2018) very similar to that seen in mouse V1 when SOMs were optogenetically silenced (Adesnik et al, 2012). And our current finding of an attenuation of gamma rhythms with feedback inactivation echoes a more recent study (Veit et al, 2017), which also found a reduction in visually evoked gamma oscillations in mouse V1 when SOMs were suppressed.…”

Stream-Specific Feedback Inputs to the Primate Primary Visual Cortex

“…The role of FF connections in shaping cortical RFs has long been recognized (Hubel and Wiesel, 1962). In contrast, little is known about the function of feedback (FB) connections, although they have been implicated in top-down modulations of neuronal responses, such as attention (Luck et al, 1997;McAdams and Reid, 2005), prediction (Friston, 2005;Rao and Ballard, 1999) and sensory context (Angelucci et al, 2017;Hupé et al, 1998;Nassi et al, 2013;Nurminen et al, 2018). One limitation to understanding the computational function of FB is that we lack information on the rules of FB connectivity to constrain models of FB function.…”

Reduced Influence of Perceptual Context in Schizophrenia: Behavioral and Neurophysiological Evidence

“…Visual contextual modulation is thought to depend on lower and higher-level processes, based on work in both animal models (Webb et al 2005;Angelucci & Bressloff 2006;Nurminen et al 2018) andhumans (Cai et al 2008;Petrov & McKee 2009;Schallmo & Murray 2016;Schallmo et al 2019) . Generally, lower level mechanisms (e.g., edge detection) are thought to manifest earlier in visual processing while higher level processes (e.g., shape integration) are thought to occur later in time.…”