Vision and Locomotion Shape the Interactions between Neuron Types in Mouse Visual Cortex

Dipoppa, Mario; Ranson, Adam; Krumin, Michael; Pachitariu, Marius; Carandini, Matteo; Harris, Kenneth D.

doi:10.1016/j.neuron.2018.03.037

Cited by 251 publications

(354 citation statements)

References 60 publications

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“…Many of these studies used anesthetized preparations, making comparisons with our results difficult, but our data are consistent with previous reports of small differences in overall activity between natural vision and complete darkness in awake animals (8) and sparse modulation of spiking in response to natural scene viewing (12,(45)(46)(47). In general, our data support the view that mean firing rates in V1 can be stabilized over both long (13) and short timescales without interfering with visual coding, which may arise through very sparse modulation of spiking and/or higher-order population dynamics (46,48,49). Despite the lack of robust changes in firing rates across the population at D-L transitions, we did observe a small subset of neurons that transiently increased their firing specifically at the appearance of visual input (Fig.…”

Section: Discussionsupporting

confidence: 92%

Rapid and active stabilization of visual cortical firing rates across light–dark transitions

Pacheco

Tilden

Grutzner

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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The dynamics of neuronal firing during natural vision are poorly understood. Surprisingly, mean firing rates of neurons in primary visual cortex (V1) of freely behaving rodents are similar during prolonged periods of light and darkness, but it is unknown whether this reflects a slow adaptation to changes in natural visual input or insensitivity to rapid changes in visual drive. Here, we use chronic electrophysiology in freely behaving rats to follow individual V1 neurons across many dark–light (D-L) and light–dark (L-D) transitions. We show that, even on rapid timescales (1 s to 10 min), neuronal activity was only weakly modulated by transitions that coincided with the expected 12-/12-h L-D cycle. In contrast, a larger subset of V1 neurons consistently responded to unexpected L-D and D-L transitions, and disruption of the regular L-D cycle with 60 h of complete darkness induced a robust increase in V1 firing on reintroduction of visual input. Thus, V1 neurons fire at similar rates in the presence or absence of natural stimuli, and significant changes in activity arise only transiently in response to unexpected changes in the visual environment. Furthermore, although mean rates were similar in light and darkness, pairwise correlations were significantly stronger during natural vision, suggesting that information about natural scenes in V1 may be more strongly reflected in correlations than individual firing rates. Together, our findings show that V1 firing rates are rapidly and actively stabilized during expected changes in visual input and are remarkably stable at both short and long timescales.

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Section: Discussionsupporting

confidence: 92%

Rapid and active stabilization of visual cortical firing rates across light–dark transitions

Pacheco

Tilden

Grutzner

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Recent work has suggested a model where VIP-INs regulate cortical circuits predominantly by inhibiting other interneurons, including the dendrite-targeting SST-INs (Pfeffer et al, 2013), thereby disinhibiting pyramidal neurons (though see (Polack et al, 2013) and (Dipoppa, 2016) for a different conclusion). We found that VIP-INs in mutants received decreased glutamatergic, but not cholinergic, synaptic input and were not appropriately activated at locomotion onset, suggesting that their impact on the local neural circuit was diminished.…”

Section: Discussionmentioning

confidence: 99%

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

Batista-Brito

Vinck

Ferguson

et al. 2017

Neuron

127

110

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GABAergic interneurons play important roles in cortical circuit development. However, there are multiple populations of interneurons and their respective developmental contributions remain poorly explored. Neuregulin 1 (NRG1) and its interneuron-specific receptor ERBB4 are critical genes for interneuron maturation. Using a conditional ErbB4 deletion, we tested the role of vasoactive intestinal peptide (VIP)-expressing interneurons in the postnatal maturation of cortical circuits in vivo. ErbB4 removal from VIP interneurons during development leads to changes in their activity, along with severe dysregulation of cortical temporal organization and state-dependence. These alterations emerge during adolescence, and mature animals in which VIP interneurons lack ErbB4 exhibit reduced cortical responses to sensory stimuli and impaired sensory learning. Our data support a key role for VIP interneurons in cortical circuit development and suggest a possible contribution to pathophysiology in neurodevelopmental disorders. These findings provide a new perspective on the role of GABAergic interneuron diversity in cortical development.

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“…Studies in awake mice have revealed that locomotion [1][2][3] , shifts of arousal [4][5][6] , motor activity 7 , and behavioral tasks [8][9][10][11][12] modulate sensory responses. These and other studies in transgenic mice have further uncovered the role of cortical neuronal subtypes 13,14 during sensory response modulation. However, it remains unknown whether cortical circuits in mice selectively enhance sensory responses to stimuli in discrete regions of space, as classically observed in primates during selective attention tasks.…”

mentioning

confidence: 81%

Spatial attention enhances network, cellular and subthreshold responses in mouse visual cortex

et al. 2020

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Internal brain states strongly modulate sensory processing during behaviour. Studies of visual processing in primates show that attention to space selectively improves behavioural and neural responses to stimuli at the attended locations. Here we develop a visual spatial task for mice that elicits behavioural improvements consistent with the effects of spatial attention, and simultaneously measure network, cellular, and subthreshold activity in primary visual cortex. During trial-by-trial behavioural improvements, local field potential (LFP) responses to stimuli detected inside the receptive field (RF) strengthen. Moreover, detection inside the RF selectively enhances excitatory and inhibitory neuron responses to task-irrelevant stimuli and suppresses noise correlations and low frequency LFP fluctuations. Whole-cell patch-clamp recordings reveal that detection inside the RF increases synaptic activity that depolarizes membrane potential responses at the behaviorally relevant location. Our study establishes that mice display fundamental signatures of visual spatial attention spanning behavioral, network, cellular, and synaptic levels, providing new insight into rapid cognitive enhancement of sensory signals in visual cortex.

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Vision and Locomotion Shape the Interactions between Neuron Types in Mouse Visual Cortex

Cited by 251 publications

References 60 publications

Rapid and active stabilization of visual cortical firing rates across light–dark transitions

Rapid and active stabilization of visual cortical firing rates across light–dark transitions

Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits

Spatial attention enhances network, cellular and subthreshold responses in mouse visual cortex

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