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

2018 ◽  
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.

scholarly journals A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

2020 ◽  
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.

scholarly journals Head Movements Control the Activity of Primary Visual Cortex in a Luminance Dependent Manner

2020 ◽  
Author(s):  
Guy Bouvier ◽  
Yuta Senzai ◽  
Massimo Scanziani
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Head Movements ◽  
Inhibitory Neurons ◽  
Dependent Manner ◽  
Ambient Light ◽  
Cortical Circuits ◽  
Cortical Layers ◽  
Visual Cortical ◽  
The Brain

AbstractThe vestibular system broadcasts head-movement related signals to sensory areas throughout the brain, including visual cortex. These signals are crucial for the brain’s ability to assess whether motion of the visual scene results from the animal’s head-movements. How head-movements impact visual cortical circuits remains, however, poorly understood. Here, we discover that ambient luminance profoundly transforms how mouse primary visual cortex (V1) processes head-movements. While in darkness, head movements result in an overall suppression of neuronal activity, in ambient light the same head movements trigger excitation across all cortical layers. This light-dependent switch in how V1 processes head-movements is controlled by somatostatin expressing (SOM) inhibitory neurons, which are excited by head movements in dark but not in light. This study thus reveals a light-dependent switch in the response of V1 to head-movements and identifies a circuit in which SOM cells are key integrators of vestibular and luminance signals.

scholarly journals Aberrant development of excitatory circuits to inhibitory neurons in the primary visual cortex after neonatal binocular enucleation

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Rongkang Deng ◽  
Joseph P. Y. Kao ◽  
Patrick O. Kanold
Keyword(s):  
Visual Cortex ◽  
Nmda Receptors ◽  
Laser Scanning ◽  
Inhibitory Neurons ◽  
Gabaergic Interneurons ◽  
Cortical Circuits ◽  
Retinal Input ◽  
Layer 4 ◽  
Ampa And Nmda Receptors ◽  
Laser Scanning Photostimulation

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.

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

2000 ◽  
Vol 83 (2) ◽  
pp. 1019-1030 ◽  
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.

scholarly journals Thalamic inputs determine functionally distinct gamma bands in mouse primary visual cortex

2020 ◽  
Author(s):  
Nicolò Meneghetti ◽  
Chiara Cerri ◽  
Elena Tantillo ◽  
Eleonora Vannini ◽  
Matteo Caleo ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Information ◽  
Narrow Band ◽  
Broad Band ◽  
Gamma Band ◽  
Neuron Network ◽  
Sensory Stimuli ◽  
Thalamic Input ◽  
Visual Contrast

AbstractGamma band is known to be involved in the encoding of visual features in the primary visual cortex (V1). Recent results in rodents V1 highlighted the presence, within a broad gamma band (BB) increasing with contrast, of a narrow gamma band (NB) peaking at ∼60 Hz suppressed by contrast and enhanced by luminance. However, the processing of visual information by the two channels still lacks a proper characterization. Here, by combining experimental analysis and modeling, we prove that the two bands are sensitive to specific thalamic inputs associated with complementary contrast ranges. We recorded local field potentials from V1 of awake mice during the presentation of gratings and observed that NB power progressively decreased from low to intermediate levels of contrast. Conversely, BB power was insensitive to low levels of contrast but it progressively increased going from intermediate to high levels of contrast. Moreover, BB response was stronger immediately after contrast reversal, while the opposite held for NB. All the aforementioned dynamics were accurately reproduced by a recurrent excitatory-inhibitory leaky integrate-and-fire network, mimicking layer IV of mouse V1, provided that the sustained and periodic component of the thalamic input were modulated over complementary contrast ranges. These results shed new light on the origin and function of the two V1 gamma bands. In addition, here we propose a simple and effective model of response to visual contrast that might help in reconstructing network dysfunction underlying pathological alterations of visual information processing.Significance StatementGamma band is a ubiquitous hallmark of cortical processing of sensory stimuli. Experimental evidence shows that in the mouse visual cortex two types of gamma activity are differentially modulated by contrast: a narrow band (NB), that seems to be rodent specific, and a standard broad band (BB), observed also in other animal models.We found that narrow band correlates and broad band anticorrelates with visual contrast in two complementary contrast ranges (low and high respectively). Moreover, BB displayed an earlier response than NB. A thalamocortical spiking neuron network model reproduced the aforementioned results, suggesting they might be due to the presence of two complementary but distinct components of the thalamic input into visual cortical circuitry.

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

eLife ◽  
2016 ◽  
Vol 5 ◽  
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.

Expression of GABAAReceptor Subunit mRNAs by Layer V Pyramidal Cells of the Rat Primary Visual Cortex

1997 ◽  
Vol 9 (4) ◽  
pp. 857-862 ◽  
Author(s):  
Diego Ruano ◽  
David Perrais ◽  
Jean Rosier ◽  
Nicole Ropert
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Pyramidal Cells ◽  
Layer V

scholarly journals Distinct Spiking Patterns of Excitatory and Inhibitory Neurons and LFP Oscillations in Prefrontal Cortex During Sensory Discrimination

2021 ◽  
Vol 12 ◽  
Author(s):  
Hua-an Tseng ◽  
Xue Han
Keyword(s):  
Prefrontal Cortex ◽  
Discrimination Task ◽  
Field Potential ◽  
Inhibitory Neurons ◽  
Sensory Stimuli ◽  
Sensory Discrimination ◽  
Related Information ◽  
Entire Duration ◽  
Excitatory Neurons ◽  
Spike Waveforms

Prefrontal cortex (PFC) are broadly linked to various aspects of behavior. During sensory discrimination, PFC neurons can encode a range of task related information, including the identity of sensory stimuli and related behavioral outcome. However, it remains largely unclear how different neuron subtypes and local field potential (LFP) oscillation features in the mouse PFC are modulated during sensory discrimination. To understand how excitatory and inhibitory PFC neurons are selectively engaged during sensory discrimination and how their activity relates to LFP oscillations, we used tetrode recordings to probe well-isolated individual neurons, and LFP oscillations, in mice performing a three-choice auditory discrimination task. We found that a majority of PFC neurons, 78% of the 711 recorded individual neurons, exhibited sensory discrimination related responses that are context and task dependent. Using spike waveforms, we classified these responsive neurons into putative excitatory neurons with broad waveforms or putative inhibitory neurons with narrow waveforms, and found that both neuron subtypes were transiently modulated, with individual neurons’ responses peaking throughout the entire duration of the trial. While the number of responsive excitatory neurons remain largely constant throughout the trial, an increasing fraction of inhibitory neurons were gradually recruited as the trial progressed. Further examination of the coherence between individual neurons and LFPs revealed that inhibitory neurons exhibit higher spike-field coherence with LFP oscillations than excitatory neurons during all aspects of the trial and across multiple frequency bands. Together, our results demonstrate that PFC excitatory neurons are continuously engaged during sensory discrimination, whereas PFC inhibitory neurons are increasingly recruited as the trial progresses and preferentially coordinated with LFP oscillations. These results demonstrate increasing involvement of inhibitory neurons in shaping the overall PFC dynamics toward the completion of the sensory discrimination task.

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