Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1

Vangeneugden, Joris; Beest, Enny H. van; Cohen, Michael X; Lorteije, Jeannette A. M.; Mukherjee, Sreedeep; Kirchberger, Lisa; Montijn, Jorrit S.; Thamizharasu, Premnath; Camillo, Daniela; Levelt, Christiaan N.; Roelfsema, Pieter; Self, Matthew W.; Heimel, J. Alexander

doi:10.1016/j.cub.2019.10.037

Cited by 43 publications

(54 citation statements)

References 46 publications

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“…7a-c). In inverse-tuned units, silencing HVAs reduced spontaneous activity and responses to classical stimuli, in particular those of smaller diameters and, as previously shown, increased the activity for large stimuli in surround suppressed units 21–23 (Fig. 5b-d; Extended Data Fig.…”

supporting

confidence: 74%

Neurons in Visual Cortex are Driven by Feedback Projections when their Feedforward Sensory Input is Missing

Keller

Roth

Scanziani

2020

Preprint

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5We sense our environment through pathways linking sensory organs to the brain. In the visual 6 system, these feedforward pathways define the classical feedforward receptive field (ffRF), the area 7 in space where visual stimuli excite a neuron 1 . The visual system also uses visual context, the visual 8 scene surrounding a stimulus, to predict the content of the stimulus 2 , and accordingly, neurons have 9 been found that are excited by stimuli outside their ffRF [3][4][5][6][7][8] . The mechanisms generating excitation to 10 stimuli outside the ffRF are, however, unclear. Here we show that feedback projections onto 11 excitatory neurons in mouse primary visual cortex (V1) generate a second receptive field driven by 12 stimuli outside the ffRF. Stimulating this feedback receptive field (fbRF) elicits slow and delayed 13 responses compared to ffRF stimulation. These responses are preferentially reduced by anesthesia 14 and, importantly, by silencing higher visual areas (HVAs). Feedback inputs from HVAs have 15 scattered receptive fields relative to their putative V1 targets enabling the generation of the fbRF. 16 Neurons with fbRFs are located in cortical layers receiving strong feedback projections and are 17 absent in the main input layer, consistent with a laminar processing hierarchy. The fbRF and the 18 ffRF are mutually antagonistic since large, uniform stimuli, covering both, suppress responses. While 19 somatostatin-expressing inhibitory neurons are driven by these large stimuli, parvalbumin and 20 vasoactive-intestinal-peptide-expressing inhibitory neurons have antagonistic fbRF and ffRF, similar 21to excitatory neurons. Therefore, feedback projections may enable neurons to use context to predict 22 and were strongly suppressed with increasing grating size (90 ± 1% suppression at 85°; mean ± SEM; 1190 33 neurons in 9 mice). Thus, consistent with previous reports, layer 2/3 excitatory neurons in V1 had a ffRF 34 diameter greater than 10° on average 9-12 and their responses were suppressed when a stimulus extended 35 beyond the ffRF to cover surrounding regions [13][14][15] . 36To determine the spatial extent of the suppressive regions, we presented a full-field grating in which a 37 portion was masked by a gray circular patch (Fig. 1a, b). We reasoned that if a large grating suppresses the 38 excitatory neuron's response because it stimulates suppressive regions surrounding the ffRF, the response 39 of the excitatory neuron should be partially recovered when a gray patch is placed on a suppressive region, 40i.e. when part of the suppressive region is not stimulated. We varied the location of the gray patch along 41 the same grid used to determine the center of the neuron's ffRF (see Methods). By averaging the responses 42 to these stimulus grids across neurons, we obtained two separate activity maps; one of the ffRF and one of 43 the suppressive regions. Unexpectedly, the peak of the map of the suppressive regions overlapped with the 44 peak of the ffRF map (Fig. 1b). This suggests that, at the population...

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supporting

confidence: 74%

Neurons in Visual Cortex are Driven by Feedback Projections when their Feedforward Sensory Input is Missing

Keller

Roth

Scanziani

2020

Preprint

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“…Instead, feedback from LM to V1 exhibited an opposite pattern with stronger connections to SOM+ cells compared to VIP+ cells, which, to our knowledge, is the first study that shows SOM+ cells are strongly activated by top-down feedback projections. Previous studies have revealed that SOM+ cells are involved in surround suppression because their activities increase with the stimulus size 41,42 , and studies in both primates 43,44 and rodents 45,46 reveal that feedback from the higher visual area contributes to surround suppression. Our finding here filled in this gap by showing that feedback from LM to V1 recruits local SOM+ interneurons.…”

Section: Discussionmentioning

confidence: 99%

Distinct organization of two cortico-cortical feedback pathways

Shen

Jiang

Scala

et al. 2020

Preprint

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Neocortical feedback is critical for processes like attention, prediction, and learning. A mechanistic understanding of its function requires deciphering its cell-type wiring logic. Recent studies revealed a disinhibitory circuit between motor and sensory areas in mice, where feedback preferentially targets vasointestinal peptide-expressing interneurons, in addition to pyramidal cells. It is unknown whether this circuit motif is a general cortico-cortical feedback organizing principle. Combining multiple simultaneous whole-cell recordings with optogenetics we found that in contrast to this wiring rule, feedback between the hierarchically organized visual areas (lateral-medial to V1) preferentially activated somatostatin-expressing interneurons. Functionally, both feedback circuits temporally sharpened feed-forward excitation by eliciting a transient increase followed by a prolonged decrease in pyramidal firing rate under sustained feed-forward input. However, under feed-forward transient input, the motor-sensory feedback facilitated pyramidal cell bursting while visual feedback increased spike time precision. Our findings argue for multiple feedback motifs implementing different dynamic non-linear operations.

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“…in its surround (Blakemore and Tobin, 1972;Hubel and Wiesel, 1965;Kapadia et al, 1999;Knierim and van Essen, 1992;Nelson and Frost, 1978). It has been shown that the mechanisms for surround suppression involve feedback connections (Angelucci et al, 2017;Nurminen et al, 2018;Vangeneugden et al, 2019), interlaminar connections (Bolz and Gilbert, 1986) and specific subtypes of inhibitory neurons (Adesnik et al, 2012;Haider et al, 2010). The tuning properties of somatostatin-expressing (SOM) inhibitory neurons (Adesnik et al, 2012) and the fact that they connect to nearly all surrounding excitatory neurons (Fino et al, 2013) make them ideal to contribute to surround suppression.…”

Section: Introductionmentioning

confidence: 99%

A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

Keller

Roth

Caudill

et al. 2020

Preprint

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Context strongly guides perception by influencing the saliency of sensory stimuli. Accordingly, sensory neurons respond differently to the same stimulus depending on the context in which the stimulus is embedded. In the visual system, the relationship between the features of the stimulus and those of the surround determine how excitatory neurons are modulated. Their responses are suppressed when center and surround share the same features but not when they are different. The mechanisms that relieve surround suppression and thereby generate contextual modulation remain unclear. Here we show that the disinhibitory circuit consisting of somatostatin-expressing (SOM) and vasoactiveintestinal-peptide-expressing (VIP) inhibitory neurons contextually modulates excitatory neurons in mouse primary visual cortex. When the stimulus and the surround share the same features, VIP neurons are inactive and SOM neurons can suppress excitatory neurons. However, when the features of the stimulus differ from those of the surround, VIP neurons are activated, thereby inhibiting SOM neurons and relieving excitatory neurons from suppression. Optogenetic silencing of VIP neurons, via disinhibition of SOM neurons, reduces the contextual modulation of excitatory neurons. We have identified a canonical cortical disinhibitory circuit which contributes to contextual modulation of excitatory neurons, and may thereby regulate perceptual saliency.

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Activity in Lateral Visual Areas Contributes to Surround Suppression in Awake Mouse V1

Cited by 43 publications

References 46 publications

Neurons in Visual Cortex are Driven by Feedback Projections when their Feedforward Sensory Input is Missing

Neurons in Visual Cortex are Driven by Feedback Projections when their Feedforward Sensory Input is Missing

Distinct organization of two cortico-cortical feedback pathways

A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

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