The essential role of recurrent processing for figure-ground perception in mice

Abstract

The segregation of figures from the background is an important step in visual perception. In primary visual cortex, figures evoke stronger activity than backgrounds during a delayed phase of the neuronal responses, but it is unknown how this figure-ground modulation (FGM) arises and whether it is necessary for perception. Here, we show, using optogenetic silencing in mice, that the delayed V1 response phase is necessary for figure-ground segregation. Neurons in higher visual areas also exhibit FGM and optogenetic silencing of higher areas reduced FGM in V1. In V1, figures elicited higher activity of vasoactive intestinal peptide–expressing (VIP) interneurons than the background, whereas figures suppressed somatostatin-positive interneurons, resulting in an increased activation of pyramidal cells. Optogenetic silencing of VIP neurons reduced FGM in V1, indicating that disinhibitory circuits contribute to FGM. Our results provide insight into how lower and higher areas of the visual cortex interact to shape visual perception.

Suppression of top-down influence decreases neuronal excitability and contrast sensitivity in the V1 cortex of cat

“…In conclusion, our results suggest that suppression of top-down influence with c-tDCS in A7 decreases neuronal activity in the V1 cortex, which is consistent with some of previous studies using neural imaging measurement 6 , 12 and some single-unit recording studies that report facilitatory top-down effects on most neurons in the V1 or low-level visual cortex 7 , 9 , 33 , 41 , and is also supported by neuronal tracing studies that identify most feedback neurons as excitatory cells 43 , 44 although top-down modulation may mediated by a mechanism of disinhibition 41 . Our result is opposite to the results of other studies that report inhibitory top-down effects of V2/V3 cortex on V1 neurons in primate and mouse 8 , 29 , 32 .…”

“…It is noteworthy that both the initial component (N1P1) and late component (P1N2) of VEPs in the V1 cortex were significantly affected by top-down suppression of A7. This is related to a recent debate about whether top-down influence can modulate the initial response of feedforward input to the V1 cortex 38 – 41 . Some authors report top-down facilitation effect on the late-phase neuronal response 41 or late ERP components (90–140 ms) 38 , whereas others find a strong attentional modulation on the initial response of VEP component (57 ms) and population response during the first wave of visual processing (< 100 ms) in the human V1 cortex 39 , 40 .…”

“…This is related to a recent debate about whether top-down influence can modulate the initial response of feedforward input to the V1 cortex 38 – 41 . Some authors report top-down facilitation effect on the late-phase neuronal response 41 or late ERP components (90–140 ms) 38 , whereas others find a strong attentional modulation on the initial response of VEP component (57 ms) and population response during the first wave of visual processing (< 100 ms) in the human V1 cortex 39 , 40 . It is likely that the top-down effect on the initial and late response components in the V1 may depend on the strength of top-down influence during different tasks 39 or the source of top-down connections from different cortical areas to the V1 cortex 42 , 43 or types of visual signals such as figure-ground stimuli 41 .…”

“…Some authors report top-down facilitation effect on the late-phase neuronal response 41 or late ERP components (90–140 ms) 38 , whereas others find a strong attentional modulation on the initial response of VEP component (57 ms) and population response during the first wave of visual processing (< 100 ms) in the human V1 cortex 39 , 40 . It is likely that the top-down effect on the initial and late response components in the V1 may depend on the strength of top-down influence during different tasks 39 or the source of top-down connections from different cortical areas to the V1 cortex 42 , 43 or types of visual signals such as figure-ground stimuli 41 . Considering that A7 has a weblike and direct projections to the V1 10 , 12 , and tDCS manipulation may trigger a large scale of top-down influence from A7, it could be reasonable that visual stimulation with full-screen size gratings may potentiate a drastic top-down effect on VEPs, even the initial VEP components, in the V1 as observed in this study.…”

Neural Circuits, Microtubule Processing, Brain’s Electromagnetic Field—Components of Self-Awareness

“…Thus, there are conditions for the circulation of impulses between neurons of higher and lower levels of afferent pathways. It has been experimentally confirmed that such oscillations occur [20][21][22][23][24].…”