Feedback generates a second receptive field in neurons of the visual cortex

Keller, Andreas; Roth, Morgane M.; Scanziani, Massimo

doi:10.1038/s41586-020-2319-4

Cited by 152 publications

(286 citation statements)

References 45 publications

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“…The main effect of silencing activity in HVAs was a decrease in activity during the late phase of the V1response, which was more pronounced for figures than the background, thereby decreasing FGM ( Figure S6). Importantly, these excitatory feedback effects imply that FGM is not caused by surround suppression and are consistent with predominantly excitatory (or disinhibitory) feedback effects on V1 activity (Huh et al, 2018;Hupé et al, 1998;Keller et al, 2020). However, a study in monkeys (Nassi et al, 2013) demonstrated that the cooling of HVAs increased V1 activity evoked by large stimuli, which suggested a suppressive influence of feedback connections.…”

Section: Discussionmentioning

confidence: 59%

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

Kirchberger

Mukherjee

et al. 2018

Preprint

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AbstractThe 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 new insight in how lower and higher areas of the visual cortex interact to shape visual perception.

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Section: Discussionmentioning

confidence: 59%

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

Kirchberger

Mukherjee

et al. 2018

Preprint

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“…the non-negative least squares (NNLS) 16,40 solution to each surrogate data set, and select from these, several data-compatible model parameters for which the network steady-states provide the best fit. This optimization takes as sole input the response data and uses no prior information on the synaptic structure, hence it is not obvious that any meaningful synaptic structure should be recoverable from such a procedure.…”

Section: Figurementioning

confidence: 99%

“…The inhibitory sub-circuit is composed of multiple elements with three types -parvalbumin-(PV), somatostatin-(SOM), and vasoactive-intestinal-peptide (VIP) expressing cells that constitute 80% of GABAergic interneurons in the mouse primary visual cortex (V1) 8 . These inhibitory cell types do not act in unison, but differentially contribute to response tuning [9][10][11][12] and to contextual [13][14][15][16][17] and behavioral-state modulations [18][19][20][21] . In particular, two of these types, SOM and VIP, engage in competitive dynamics whose outcome directly regulates pyramidal cell activity via inhibition or disinhibition.…”

Section: Introductionmentioning

confidence: 99%

Common rules underlying optogenetic and behavioral modulation of responses in multi-cell-type V1 circuits

Palmigiano

Fumarola

Mossing

et al. 2020

Preprint

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Identifying the regime in which the cortical microcircuit operates is a prerequisite to determine the mechanisms that mediate its response to stimulus. Classic modeling work has started to characterize this regime through the study of perturbations, but an encompassing perspective that links the full ensemble of the network’s response to appropriate descriptors of the cortical operating regime is still lacking. Here we develop a class of mathematically tractable models that exactly describe the modulation of the distribution of cell-type-specific calcium-imaging activity with the contrast of a visual stimulus. The model’s fit recovers signatures of the connectivity structure found in mouse visual cortex. Analysis of this structure subsequently reveal parameter-independent relations between the responses of different cell types to perturbations and each interneuron’s role in circuit-stabilization. Leveraging recent theoretical approaches, we derive explicit expressions for the distribution of responses to partial perturbations which reveal a novel, counter-intuitive effect in the sign of response functions.

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“…In addition, the apical dendritic tufts of cortical pyramidal neurons in layer 1 receive top-down feedback inputs from higher-order cortical areas (Rockland and Pandya, 1979;Felleman and Van Essen, 1991;Cauller et al, 1998) and inputs from thalamocortical projections (Roth et al, 2016). These long-range excitatory inputs are thought to provide contextual information to primary cortex neurons, regulating the integration and gain of sensory-evoked responses (Schiller et al, 1997;Larkum and Zhu, 2002;Larkum et al, 2004;Wang et al, 2007;Nassi et al, 2013;Keller et al, 2020). In addition, pyramidal neurons also receive inhibitory inputs on both apical dendritic shafts and spines (refs) that are robustly modulated by arousal and locomotion (Fu et al, 2014a;Pakan et al, 2016;Dipoppa et al, 2018) and can modulate excitatory synaptic inputs to spines (Chiu et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Developmental loss of ErbB4 in PV interneurons disrupts state-dependent cortical circuit dynamics

Batista-Brito

Majumdar

Nuno

et al. 2020

Preprint

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GABAergic inhibition plays an important role in the establishment and maintenance of cortical circuits during development. Neuregulin 1 (Nrg1) and its interneuron-specific receptor ErbB4 are key elements of a signaling pathway critical for the maturation and proper synaptic connectivity of interneurons. Using conditional deletions of the ERBB4 gene in mice, we tested the role of this signaling pathway at two developmental timepoints in parvalbumin-expressing (PV) interneurons, the largest subpopulation of cortical GABAergic cells. Loss of ErbB4 in PV interneurons during embryonic, but not late postnatal, development leads to alterations in the activity of excitatory and inhibitory cortical neurons, along with severe disruption of cortical temporal organization. These impairments emerge by the end of the second postnatal week, prior to the complete maturation of the PV interneurons themselves. Early loss of ErbB4 in PV interneurons also results in profound dysregulation of excitatory pyramidal neuron dendritic architecture and a redistribution of spine density at the apical dendritic tuft. In association with these deficits, excitatory cortical neurons exhibit normal tuning for sensory inputs, but a loss of state-dependent modulation of the gain of sensory responses. Together these data support a key role for early developmental Nrg1/ErbB4 signaling in PV interneurons as powerful mechanism underlying the maturation of both the inhibitory and excitatory components of cortical circuits.

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Feedback generates a second receptive field in neurons of the visual cortex

Cited by 152 publications

References 45 publications

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

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

Common rules underlying optogenetic and behavioral modulation of responses in multi-cell-type V1 circuits

Developmental loss of ErbB4 in PV interneurons disrupts state-dependent cortical circuit dynamics

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