Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex

AbstractThe development of GABAergic interneurons is important for the functional maturation of cortical circuits. After migrating into the cortex, GABAergic interneurons start to receive glutamatergic connections from cortical excitatory neurons and thus gradually become integrated into cortical circuits. These glutamatergic connections are mediated by glutamate receptors including AMPA and NMDA receptors and the ratio of AMPA to NMDA receptors decreases during development. Since previous studies have shown that retinal input can regulate the early development of connections along the visual pathway, we investigated if the maturation of glutamatergic inputs to GABAergic interneurons in the visual cortex requires retinal input. We mapped the spatial pattern of glutamatergic connections to layer 4 (L4) GABAergic interneurons in mouse visual cortex at around postnatal day (P) 16 by laser-scanning photostimulation and investigated the effect of binocular enucleations at P1/P2 on these patterns. Gad2-positive interneurons in enucleated animals showed an increased fraction of AMPAR-mediated input from L2/3 and a decreased fraction of input from L5/6. Parvalbumin-expressing (PV) interneurons showed similar changes in relative connectivity. NMDAR-only input was largely unchanged by enucleation. Our results show that retinal input sculpts the integration of interneurons into V1 circuits and suggest that the development of AMPAR- and NMDAR-only connections might be regulated differently.

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Dynamic Properties of Recurrent Inhibition in Primary Visual Cortex: Contrast and Orientation Dependence of Contextual Effects

Journal of Neurophysiology ◽

10.1152/jn.2000.83.2.1019 ◽

2000 ◽

Vol 83 (2) ◽

pp. 1019-1030 ◽

Cited By ~ 61

Author(s):

Valentin Dragoi ◽

Mriganka Sur

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Dynamic Properties ◽

Orientation Dependence ◽

Recurrent Inhibition ◽

Inhibitory Neurons ◽

Classical Receptive Field ◽

Contextual Interactions ◽

Receptive Field Center

A fundamental feature of neural circuitry in the primary visual cortex (V1) is the existence of recurrent excitatory connections between spiny neurons, recurrent inhibitory connections between smooth neurons, and local connections between excitatory and inhibitory neurons. We modeled the dynamic behavior of intermixed excitatory and inhibitory populations of cells in V1 that receive input from the classical receptive field (the receptive field center) through feedforward thalamocortical afferents, as well as input from outside the classical receptive field (the receptive field surround) via long-range intracortical connections. A counterintuitive result is that the response of oriented cells can be facilitated beyond optimal levels when the surround stimulus is cross-oriented with respect to the center and suppressed when the surround stimulus is iso-oriented. This effect is primarily due to changes in recurrent inhibition within a local circuit. Cross-oriented surround stimulation leads to a reduction of presynaptic inhibition and a supraoptimal response, whereas iso-oriented surround stimulation has the opposite effect. This mechanism is used to explain the orientation and contrast dependence of contextual interactions in primary visual cortex: responses to a center stimulus can be both strongly suppressed and supraoptimally facilitated as a function of surround orientation, and these effects diminish as stimulus contrast decreases.

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Functional selectivity and specific connectivity of inhibitory neurons in primary visual cortex

10.1101/294835 ◽

2018 ◽

Cited By ~ 25

Author(s):

Petr Znamenskiy ◽

Mean-Hwan Kim ◽

Dylan R. Muir ◽

Maria Florencia Iacaruso ◽

Sonja B. Hofer ◽

...

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Pyramidal Cells ◽

Fine Tuning ◽

Inhibitory Neurons ◽

Local Network ◽

Cortical Circuits ◽

Sensory Stimuli ◽

Excitatory Neurons ◽

Strong Excitation

In the cerebral cortex, the interaction of excitatory and inhibitory synaptic inputs shapes the responses of neurons to sensory stimuli, stabilizes network dynamics1 and improves the efficiency and robustness of the neural code2–4. Excitatory neurons receive inhibitory inputs that track excitation5–8. However, how this co-tuning of excitation and inhibition is achieved by cortical circuits is unclear, since inhibitory interneurons are thought to pool the inputs of nearby excitatory cells and provide them with non-specific inhibition proportional to the activity of the local network9–13. Here we show that although parvalbumin-expressing (PV) inhibitory cells in mouse primary visual cortex make connections with the majority of nearby pyramidal cells, the strength of their synaptic connections is structured according to the similarity of the cells’ responses. Individual PV cells strongly inhibit those pyramidal cells that provide them with strong excitation and share their visual selectivity. This fine-tuning of synaptic weights supports co-tuning of inhibitory and excitatory inputs onto individual pyramidal cells despite dense connectivity between inhibitory and excitatory neurons. Our results indicate that individual PV cells are preferentially integrated into subnetworks of inter-connected, co-tuned pyramidal cells, stabilising their recurrent dynamics. Conversely, weak but dense inhibitory connectivity between subnetworks is sufficient to support competition between them, de-correlating their output. We suggest that the history and structure of correlated firing adjusts the weights of both inhibitory and excitatory connections, supporting stable amplification and selective recruitment of cortical subnetworks.

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Dopamine Receptor Expression Among Local and Visual Cortex-Projecting Frontal Eye Field Neurons

Cerebral Cortex ◽

10.1093/cercor/bhz078 ◽

2019 ◽

Vol 30 (1) ◽

pp. 148-164 ◽

Cited By ~ 1

Author(s):

Adrienne Mueller ◽

Rebecca M Krock ◽

Steven Shepard ◽

Tirin Moore

Keyword(s):

Visual Cortex ◽

Pyramidal Neurons ◽

Receptor Expression ◽

Inhibitory Neurons ◽

Extrastriate Cortex ◽

Frontal Eye Field ◽

D2 Dopamine Receptors ◽

Dopaminergic Modulation ◽

Eye Field ◽

Parvalbumin Neurons

Abstract Dopaminergic modulation of prefrontal cortex plays an important role in numerous cognitive processes, including attention. The frontal eye field (FEF) is modulated by dopamine and has an established role in visual attention, yet the underlying circuitry upon which dopamine acts is not known. We compared the expression of D1 and D2 dopamine receptors (D1Rs and D2Rs) across different classes of FEF neurons, including those projecting to dorsal or ventral extrastriate cortex. First, we found that both D1Rs and D2Rs are more prevalent on pyramidal neurons than on several classes of interneurons and are particularly prevalent on putatively long-range projecting pyramidals. Second, higher proportions of pyramidal neurons express D1Rs than D2Rs. Third, overall a higher proportion of inhibitory neurons expresses D2Rs than D1Rs. Fourth, among inhibitory interneurons, a significantly higher proportion of parvalbumin+ neurons expresses D2Rs than D1Rs, and a significantly higher proportion of calbindin+ neurons expresses D1Rs than D2Rs. Finally, compared with D2Rs, virtually all of the neurons with identified projections to both dorsal and ventral extrastriate visual cortex expressed D1Rs. Our results demonstrate that dopamine tends to act directly on the output of the FEF and that dopaminergic modulation of top-down projections to visual cortex is achieved predominately via D1Rs.

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Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex

eLife ◽

10.7554/elife.14985 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 107

Author(s):

Janelle MP Pakan ◽

Scott C Lowe ◽

Evelyn Dylda ◽

Sander W Keemink ◽

Stephen P Currie ◽

...

Keyword(s):

Visual Cortex ◽

Pyramidal Neurons ◽

Visual Stimulation ◽

Inhibitory Neurons ◽

Behavioral State ◽

Visual Responses ◽

Cell Type ◽

Sensory Stimuli ◽

Context Dependent

Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.

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Target Interneuron Preference in Thalamocortical Pathways Determines the Temporal Structure of Cortical Responses

Cerebral Cortex ◽

10.1093/cercor/bhy148 ◽

2018 ◽

Vol 29 (7) ◽

pp. 2815-2831 ◽

Cited By ~ 2

Author(s):

Y Audrey Hay ◽

Jérémie Naudé ◽

Philippe Faure ◽

Bertrand Lambolez

Keyword(s):

Temporal Structure ◽

Sensory Information ◽

Response Duration ◽

Cortical Response ◽

Inhibitory Neurons ◽

Thalamic Nuclei ◽

Response Dynamics ◽

Mean Field Model ◽

Local Circuits ◽

Feedforward Inhibition

Abstract Sensory processing relies on fast detection of changes in environment, as well as integration of contextual cues over time. The mechanisms by which local circuits of the cerebral cortex simultaneously perform these opposite processes remain obscure. Thalamic “specific” nuclei relay sensory information, whereas “nonspecific” nuclei convey information on the environmental and behavioral contexts. We expressed channelrhodopsin in the ventrobasal specific (sensory) or the rhomboid nonspecific (contextual) thalamic nuclei. By selectively activating each thalamic pathway, we found that nonspecific inputs powerfully activate adapting (slow-responding) interneurons but weakly connect fast-spiking interneurons, whereas specific inputs exhibit opposite interneuron preference. Specific inputs thereby induce rapid feedforward inhibition that limits response duration, whereas, in the same cortical area, nonspecific inputs elicit delayed feedforward inhibition that enables lasting recurrent excitation. Using a mean field model, we confirm that cortical response dynamics depends on the type of interneuron targeted by thalamocortical inputs and show that efficient recruitment of adapting interneurons prolongs the cortical response and allows the summation of sensory and contextual inputs. Hence, target choice between slow- and fast-responding inhibitory neurons endows cortical networks with a simple computational solution to perform both sensory detection and integration.

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Delayed plasticity of inhibitory neurons in developing visual cortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0806159105 ◽

2008 ◽

Vol 105 (43) ◽

pp. 16797-16802 ◽

Cited By ~ 75

Author(s):

S. P. Gandhi ◽

Y. Yanagawa ◽

M. P. Stryker

Keyword(s):

Visual Cortex ◽

Inhibitory Neurons

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Sensory-driven and spontaneous gamma oscillations engage distinct cortical circuitry

Journal of Neurophysiology ◽

10.1152/jn.00137.2015 ◽

2016 ◽

Vol 115 (4) ◽

pp. 1821-1835 ◽

Cited By ~ 16

Author(s):

Cristin G. Welle ◽

Diego Contreras

Keyword(s):

Visual Cortex ◽

Visual Stimulation ◽

Oscillation Amplitude ◽

Gamma Oscillations ◽

Gamma Oscillation ◽

Inhibitory Neurons ◽

Sensory Representation ◽

Cortical Circuitry ◽

Mouse Visual Cortex

Gamma oscillations are a robust component of sensory responses but are also part of the background spontaneous activity of the brain. To determine whether the properties of gamma oscillations in cortex are specific to their mechanism of generation, we compared in mouse visual cortex in vivo the laminar geometry and single-neuron rhythmicity of oscillations produced during sensory representation with those occurring spontaneously in the absence of stimulation. In mouse visual cortex under anesthesia (isoflurane and xylazine), visual stimulation triggered oscillations mainly between 20 and 50 Hz, which, because of their similar functional significance to gamma oscillations in higher mammals, we define here as gamma range. Sensory representation in visual cortex specifically increased gamma oscillation amplitude in the supragranular (L2/3) and granular (L4) layers and strongly entrained putative excitatory and inhibitory neurons in infragranular layers, while spontaneous gamma oscillations were distributed evenly through the cortical depth and primarily entrained putative inhibitory neurons in the infragranular (L5/6) cortical layers. The difference in laminar distribution of gamma oscillations during the two different conditions may result from differences in the source of excitatory input to the cortex. In addition, modulation of superficial gamma oscillation amplitude did not result in a corresponding change in deep-layer oscillations, suggesting that superficial and deep layers of cortex may utilize independent but related networks for gamma generation. These results demonstrate that stimulus-driven gamma oscillations engage cortical circuitry in a manner distinct from spontaneous oscillations and suggest multiple networks for the generation of gamma oscillations in cortex.

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A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

10.1101/2020.01.31.929166 ◽

2020 ◽

Cited By ~ 4

Author(s):

Andreas J. Keller ◽

Mario Dipoppa ◽

Morgane M. Roth ◽

Matthew S. Caudill ◽

Alessandro Ingrosso ◽

...

Keyword(s):

Visual Cortex ◽

Vasoactive Intestinal Peptide ◽

Primary Visual Cortex ◽

Computational Modelling ◽

Visual Scene ◽

Inhibitory Neurons ◽

Contextual Modulation ◽

Sensory Stimuli ◽

Excitatory Neurons ◽

Mouse Visual Cortex

Context guides perception by influencing the saliency of sensory stimuli. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The mechanisms that remove suppression when stimulus and surround differ remain unclear. Here we use optical recordings, manipulations, and computational modelling to show that a disinhibitory circuit consisting of vasoactive-intestinal-peptide-expressing (VIP) and somatostatin-expressing (SOM) inhibitory neurons modulates responses in mouse visual cortex depending on the similarity between stimulus and surround. When the stimulus and the surround are similar, VIP neurons are inactive and SOM neurons suppress excitatory neurons. However, when the stimulus and the surround differ, VIP neurons are active, thereby inhibiting SOM neurons and relieving excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit which contributes to contextual modulation and may regulate perceptual saliency.

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Dynamic representation of partially occluded objects in primate prefrontal and visual cortex

eLife ◽

10.7554/elife.25784 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 14

Author(s):

Amber M Fyall ◽

Yasmine El-Shamayleh ◽

Hannah Choi ◽

Eric Shea-Brown ◽

Anitha Pasupathy

Keyword(s):

Visual Cortex ◽

Response Dynamics ◽

Dynamic Interactions ◽

Area V4 ◽

Dynamic Representation ◽

Occluded Objects ◽

Response Onset ◽

Shape Selective ◽

Partially Occluded ◽

V4 Neurons

Successful recognition of partially occluded objects is presumed to involve dynamic interactions between brain areas responsible for vision and cognition, but neurophysiological evidence for the involvement of feedback signals is lacking. Here, we demonstrate that neurons in the ventrolateral prefrontal cortex (vlPFC) of monkeys performing a shape discrimination task respond more strongly to occluded than unoccluded stimuli. In contrast, neurons in visual area V4 respond more strongly to unoccluded stimuli. Analyses of V4 response dynamics reveal that many neurons exhibit two transient response peaks, the second of which emerges after vlPFC response onset and displays stronger selectivity for occluded shapes. We replicate these findings using a model of V4/vlPFC interactions in which occlusion-sensitive vlPFC neurons feed back to shape-selective V4 neurons, thereby enhancing V4 responses and selectivity to occluded shapes. These results reveal how signals from frontal and visual cortex could interact to facilitate object recognition under occlusion.

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