Distinct Balance of Excitation and Inhibition in an Interareal Feedforward and Feedback Circuit of Mouse Visual Cortex

Yang, Weiguo; Carrasquillo, Yarimar; Hooks, Bryan M.; Nerbonne, Jeanne M.; Burkhalter, Andreas

doi:10.1523/jneurosci.2515-13.2013

Cited by 100 publications

(124 citation statements)

References 60 publications

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“…Our results suggest that the mechanisms underlying BF-induced response gain in V1 are not present in LM and that increased V1 responsiveness is not propagated to LM. A possible mechanism that could account for both phenomena would be that feedforward inhibition dominates in the V1-LM pathway (Yang et al, 2013). However, given that we found that the visually evoked firing rate of PV neurons in LM actually decreased during BF stimulation, this possibility is unlikely.…”

Section: Areal Differences In Response To Bf Stimulationmentioning

confidence: 88%

“…Alternatively, regional differences in the expression of signaling molecules such as the muscarinic type 2 acetylcholine receptor (m2AChR) may contribute to response differences and a second, distinct mechanism could be involved in dampening V1-LM propagation. m2AChR expression is lower in LM compared with V1 (Wang et al, 2012;Ji et al, 2015) and activation of presynaptic m2AChRs expressed in PV neuron inhibitory terminals synapsing onto excitatory neurons are known to inhibit the release of GABA (Muñoz and Rudy, 2014). Therefore, the absence of an m2AChR-mediated boosting effect in LM could explain why, although present, stimulation of BF fibers does not result in increased excitability within LM.…”

Section: Areal Differences In Response To Bf Stimulationmentioning

confidence: 98%

“…Recent studies establish that the visual cortex in mice is hierarchically arranged into functional areas that have distinct preferences for visual features (Wang and Burkhalter, 2007;Andermann et al, 2011;Marshel et al, 2011;Wang et al, 2012;Glickfeld et al, 2013). These higher-order areas provide top-down feedback to primary visual cortex (V1), feedback that is well positioned to convey information regarding context and previously learned statistical features (Gilbert and Li, 2013;Nassi et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…To address this, we developed an assay to quantify the contribution of the most prominent source of cortical feedback, the lateral medial area (LM) (Wang and Burkhalter, 2007;Wang et al, 2012), on V1 responsiveness in combination with subcortical BF activation. We found LM facilitates visual responses in L2/3 excitatory neurons by ϳ20%.…”

Section: Introductionmentioning

confidence: 99%

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Top-Down-Mediated Facilitation in the Visual Cortex Is Gated by Subcortical Neuromodulation

et al. 2016

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Response properties in primary sensory cortices are highly dependent on behavioral state. For example, the nucleus basalis of the forebrain plays a critical role in enhancing response properties of excitatory neurons in primary visual cortex (V1) during active exploration and learning. Given the strong reciprocal connections between hierarchically arranged cortical regions, how are increases in sensory response gain constrained to prevent runaway excitation? To explore this, we used in vivo two-photon guided cell-attached recording in conjunction with spatially restricted optogenetic photo-inhibition of higher-order visual cortex in mice. We found that the principle feedback projection to V1 originating from the lateral medial area (LM) facilitated visual responses in layer 2/3 excitatory neurons by ϳ20%. This facilitation was reduced by half during basal forebrain activation due to differential response properties between LM and V1. Our results demonstrate that basal-forebrain-mediated increases in response gain are localized to V1 and are not propagated to LM and establish that subcortical modulation of visual cortex is regionally distinct.

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Section: Areal Differences In Response To Bf Stimulationmentioning

confidence: 88%

Section: Areal Differences In Response To Bf Stimulationmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Top-Down-Mediated Facilitation in the Visual Cortex Is Gated by Subcortical Neuromodulation

et al. 2016

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“…Physiologically, however, the responses of pyramidal cells to feedforward inputs are opposed by stronger inhibition than the responses to feedback inputs (Shao and Burkhalter 1996;Dong et al 2004b). The reasons for the pathway-specific excitatory/inhibitory balance are that feedforward inputs to parvalbumin-expressing neurons are relatively stronger than to pyramidal cells whereas feedback inputs to both types of cells are similar (Yang et al 2013). The stronger excitation of parvalbumin neurons is probably due to signaling via calcium-permeable GluR2-lacking AMPA receptors that elicit large quantal amplitude responses with fast kinetics (Hull et al 2009).…”

Section: Synaptic Organization Of Feedforward and Feedback Connectionsmentioning

confidence: 99%

The Network for Intracortical Communication in Mouse Visual Cortex

Burkhalter¹

2016

Micro-, Meso- And Macro-Connectomics of the Brain

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New techniques for identifying cell types, tracing their synaptic partners, imaging and manipulating their activity in behaving organisms have made mice a widely used model for linking brain circuits to behavior. Most behaviors are tied to vision: identifying objects, guiding movements of body parts, navigating through the environment, and even social interactions. Reason enough to focus on the mouse visual cortex. To find our way around in the occipital cortex, we needed a map. We took a classic approach and traced in the same animal the outputs from multiple retinotopic sites of primary visual cortex (V1) and compared the relative location of projections in the extrastriate cortex. We found nine extrastriate maps and showed by single unit recordings that each of the connectional maps contained visually responsive neurons whose receptive fields were mapped in orderly fashion and completely covered the visual field. Remarkably, a tiny region of one sixth of a dime contained a two-to three-times larger number of areas than the highly developed somatosensory and auditory cortices. By tracing the connections, we found that each of the ten visual areas projected to 25-35 cortical targets and interconnected virtually all of the areas reciprocally with one another. Although the binary graph density of the connection matrix was nearly complete, the connection strengths between areas within the ventral and dorsal cortex differed, indicating that the information from V1 flowed into distinct but interconnected streams. Unit recordings and calcium imaging studies showed that the ventral and dorsal streams processed different spatiotemporal information, which aligned with known properties of streams in primates. Analyses of the laminar patterns of interareal projections showed that areas were organized at multiple levels, suggesting that each stream represented a processing hierarchy.

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