scholarly journals NMDAR-dependent emergence of behavioral representation in primary visual cortex

2019 ◽  
Author(s):  
Alicja Puścian ◽  
Hadas Benisty ◽  
Michael J. Higley

AbstractNeocortical sensory areas are generally thought to faithfully represent external stimuli. However, a growing body of evidence suggests that cortical networks exhibit considerable functional plasticity over multiple temporal scales, allowing them to modify their output to reflect ongoing behavioral demands. Nevertheless, the dynamics of sensory and non-sensory representations during acquisition of stimulus-guided behavior are not well understood. We performed longitudinal 2-photon imaging of activity in primary visual cortex (V1) of mice learning a conditioned eyeblink task. We found that both excitatory and inhibitory neurons robustly encode the visual stimulus throughout training despite a significant experience-dependent reduction in response magnitude. In contrast, both pyramidal neurons and parvalbumin-expressing interneurons exhibit emergence of behavioral representation during learning. The plasticity of visual response magnitude and behavioral representation is abolished following loss of NMDA-type glutamate receptors. Overall, our findings demonstrate that V1 networks can dynamically multiplex distinct behaviorally relevant representations over the course of learning.

2000 ◽  
Vol 83 (2) ◽  
pp. 1019-1030 ◽  
Author(s):  
Valentin Dragoi ◽  
Mriganka Sur

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.


2018 ◽  
Author(s):  
Petr Znamenskiy ◽  
Mean-Hwan Kim ◽  
Dylan R. Muir ◽  
Maria Florencia Iacaruso ◽  
Sonja B. Hofer ◽  
...  

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.


2019 ◽  
Vol 30 (1) ◽  
pp. 148-164 ◽  
Author(s):  
Adrienne Mueller ◽  
Rebecca M Krock ◽  
Steven Shepard ◽  
Tirin Moore

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.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Janelle MP Pakan ◽  
Scott C Lowe ◽  
Evelyn Dylda ◽  
Sander W Keemink ◽  
Stephen P Currie ◽  
...  

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.


Author(s):  
Andreas J. Keller ◽  
Mario Dipoppa ◽  
Morgane M. Roth ◽  
Matthew S. Caudill ◽  
Alessandro Ingrosso ◽  
...  

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.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Daniel J Millman ◽  
Gabriel Koch Ocker ◽  
Shiella Caldejon ◽  
India Kato ◽  
Josh D Larkin ◽  
...  

Vasoactive intestinal peptide-expressing (VIP) interneurons in the cortex regulate feedback inhibition of pyramidal neurons through suppression of somatostatin-expressing (SST) interneurons and, reciprocally, SST neurons inhibit VIP neurons. Although VIP neuron activity in the primary visual cortex (V1) of mouse is highly correlated with locomotion, the relevance of locomotion-related VIP neuron activity to visual coding is not known. Here we show that VIP neurons in mouse V1 respond strongly to low contrast front-to-back motion that is congruent with self-motion during locomotion but are suppressed by other directions and contrasts. VIP and SST neurons have complementary contrast tuning. Layer 2/3 contains a substantially larger population of low contrast preferring pyramidal neurons than deeper layers, and layer 2/3 (but not deeper layer) pyramidal neurons show bias for front-to-back motion specifically at low contrast. Network modeling indicates that VIP-SST mutual antagonism regulates the gain of the cortex to achieve sensitivity to specific weak stimuli without compromising network stability.


2021 ◽  
Author(s):  
Wei Wen ◽  
Gina Turrigiano

Homeostatic plasticity maintains network stability by adjusting excitation, inhibition, or the intrinsic excitability of neurons, but the developmental regulation and coordination of these distinct forms of homeostatic plasticity remains poorly understood. A major contributor to this information gap is the lack of a uniform paradigm for chronically manipulating activity at different developmental stages. To overcome this limitation, we utilized Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) to directly suppress neuronal activity in layer (L) 2/3 of mouse primary visual cortex (V1) at two important developmental timepoints: the classic visual system critical period (CP, P24-29), and adulthood (P45-55). We show that 24 hours of DREADD-mediated activity suppression simultaneously induces excitatory synaptic scaling up and intrinsic homeostatic plasticity in L2/3 pyramidal neurons during the CP, consistent with previous observations using prolonged visual deprivation. Importantly, manipulations known to block these forms of homeostatic plasticity when induced pharmacologically or via visual deprivation also prevented DREADD-induced homeostatic plasticity. We next used the same paradigm to suppress activity in adult animals. Surprisingly, while excitatory synaptic scaling persisted into adulthood, intrinsic homeostatic plasticity was completely absent. Finally, we found that homeostatic changes in quantal inhibitory input onto L2/3 pyramidal neurons were absent during the CP but present in adults. Thus, the same population of neurons can express distinct sets of homeostatic plasticity mechanisms at different development stages. Our findings suggest that homeostatic forms of plasticity can be recruited in a modular manner according to the evolving needs of a developing neural circuit.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Atena Sajedin ◽  
Mohammad Bagher Menhaj ◽  
Abdol-Hossein Vahabie ◽  
Stefano Panzeri ◽  
Hossein Esteky

AbstractAttention greatly influences sensory neural processing by enhancing firing rates of neurons that represent the attended stimuli and by modulating their tuning properties. The cholinergic system is believed to partly mediate the attention contingent improvement of cortical processing by influencing neuronal excitability, synaptic transmission and neural network characteristics. Here, we used a biophysically based model to investigate the mechanisms by which cholinergic system influences sensory information processing in the primary visual cortex (V1) layer 4C. The physiological properties and architectures of our model were inspired by experimental data and include feed-forward input from dorsal lateral geniculate nucleus that sets up orientation preference in V1 neural responses. When including a cholinergic drive, we found significant sharpening in orientation selectivity, desynchronization of LFP gamma power and spike-field coherence, decreased response variability and correlation reduction mostly by influencing intracortical interactions and by increasing inhibitory drive. Our results indicated that these effects emerged due to changes specific to the behavior of the inhibitory neurons. The behavior of our model closely resembles the effects of attention on neural activities in monkey V1. Our model suggests precise mechanisms through which cholinergic modulation may mediate the effects of attention in the visual cortex.


1997 ◽  
Vol 14 (1) ◽  
pp. 83-88 ◽  
Author(s):  
Silvia N.M. Reid ◽  
Nigel W. Daw

AbstractSingle neurons were recorded in cat primary visual cortex, and the effect of iontophoresis of the metabotropic glutamate agonist 1S,3R-aminocyclopentane-1.3-dicarboxylic acid (ACPD) was observed. In nearly all cases (41/43), ACPD reduced the visual response. In some cases ACPD also reduced spontaneous activity (24/43), and in other cases ACPD increased spontaneous activity (18/43). Increases were generally seen in infragranular layers (V and VI), and decreases in supragranular layers (II and III). The reduction in the visual response was also largest in supragranular layers. We conclude that activation of metabotropic glutamate receptors has both facilitatory and depressive effects in visual cortex, and the effect depends on the layer of the cell recorded.


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