A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex (original) (raw)
Related papers
biorxiv, 2017
Cortical neurons often respond to identical sensory stimuli with large variability. However, under certain conditions, the same neurons can also respond highly reliably. The circuit mechanisms that contribute to this modulation, and their influence on behavior remains unknown. Here we used novel double transgenic mice, dual-wavelength calcium imaging and temporally selective optical perturbation to identify an inhibitory neural circuit in visual cortex that can modulate the reliability of pyramidal neurons to naturalistic visual stimuli. Our results, supported by computational models, suggest that somatostatin interneurons (SST-INs) increase pyramidal neuron reliability by suppressing parvalbumin interneurons (PV-INs) via the inhibitory SSTàPV circuit. Using a novel movie classification task, we further show that, by reducing variability, activating SST-INs can improve the ability of mice to discriminate between ambiguous stimuli.
A neural circuit for spatial summation in visual cortex
Nature, 2012
The response of cortical neurons to a sensory stimulus is modulated by the context. In the visual cortex, for example, stimulation of a pyramidal cell's receptive field surround can attenuate the cell's response to a stimulus in its receptive field's center, a phenomenon called surround suppression. Whether cortical circuits contribute to surround suppression or whether the phenomenon is entirely relayed from earlier stages of visual processing is controversial. Here we discover that, in contrast to pyramidal cells, the response of somatostatin expressing inhibitory neurons (SOMs) in the superficial layers of the mouse visual cortex increases with stimulation of the receptive field surround. This difference results from SOMs' preferential excitation by horizontal cortical axons. By perturbing SOMs' activity, we demonstrate that these neurons contribute to pyramidal cells' surround suppression. These results establish a cortical circuit for surround suppression and attribute a particular function to a genetically defined type of inhibitory neuron.
Neural responses to a localized visual stimulus are modulated by the content of its surrounding. This phenomenon manifests in several forms of contextual modulation, including three interrelated properties of the visual cortex: surround suppression, inverse response and surround facilitation. We devise a unified biologically realistic circuit model accounting for all these phenomena and show that i) surround suppression in L2/3 is only partially due to the recruitment of lateral inhibition; ii) long-range feedback projections are necessary for inverse response and iii) the width of the response profile in the feedback layer determines inverse size tuning. The model predicts the modulations induced by silencing somatostatin-expressing cells or higher visual areas or changing the stimulus contrast. These predictions are consistent with the experimental observations when available and can be tested in existing setups otherwise. We then show the robustness of the identified mechanisms i...
Neuronal circuitry for stimulus selection in the visual system
Visual objects naturally compete for the brain’s attention, and selecting just one of them for a behavioural response is often crucial for the animal’s survival1. The neural correlate of such stimulus prioritisation might take the form of a saliency map by which responses to one target are enhanced relative to distractors in other parts of the visual field2. Single-cell responses consistent with this type of computation have been observed in the tectum of primates, birds, turtles and lamprey2–7. However, the exact circuit implementation has remained unclear. Here we investigated the underlying neuronal mechanism presenting larval zebrafish with two simultaneous looming stimuli, each of which was able to trigger directed escapes on their own. Behaviour tracking revealed that the fish respond to these competing stimuli predominantly with a winner-take-all strategy. Using brain-wide functional recordings, we discovered neurons in the tectum whose responses to the target stimulus were n...
Orientation-Tuned Surround Suppression in Mouse Visual Cortex
Journal of Neuroscience, 2014
The firing rates of neurons in primary visual cortex (V1) are suppressed by large stimuli, an effect known as surround suppression. In cats and monkeys, the strength of suppression is sensitive to orientation; responses to regions containing uniform orientations are more suppressed than those containing orientation contrast. This effect is thought to be important for scene segmentation, but the underlying neural mechanisms are poorly understood. We asked whether it is possible to study these mechanisms in the visual cortex of mice, because of recent advances in technology for studying the cortical circuitry in mice. It is unknown whether neurons in mouse V1 are sensitive to orientation contrast. We measured the orientation selectivity of surround suppression in the different layers of mouse V1. We found strong surround suppression in layer 4 and the superficial layers, part of which was orientation tuned: iso-oriented surrounds caused more suppression than cross-oriented surrounds. Surround suppression was delayed relative to the visual response and orientation-tuned suppression was delayed further, suggesting two separate suppressive mechanisms. Previous studies proposed that surround suppression depends on the activity of inhibitory somatostatin-positive interneurons in the superficial layers. To test the involvement of the superficial layers we topically applied lidocaine. Silencing of the superficial layers did not prevent orientation-tuned suppression in layer 4. These results show that neurons in mouse V1, which lacks orientation columns, show orientation-dependent surround suppression in layer 4 and the superficial layers and that surround suppression in layer 4 does not require contributions from neurons in the superficial layers. Self et al. • Orientation-Tuned Suppression J. Neurosci., July 9, 2014 • 34(28):9290 -9304 • 9291 Self et al. • Orientation-Tuned Suppression J. Neurosci., July 9, 2014 • 34(28):9290 -9304 • 9303
2020
We sense our environment through pathways linking sensory organs to the brain. In the visual system, these feedforward pathways define the classical feedforward receptive field (ffRF), the area in space where visual stimuli excite a neuron1. The visual system also uses visual context, the visual scene surrounding a stimulus, to predict the content of the stimulus2, and accordingly, neurons have been found that are excited by stimuli outside their ffRF3–8. The mechanisms generating excitation to stimuli outside the ffRF are, however, unclear. Here we show that feedback projections onto excitatory neurons in mouse primary visual cortex (V1) generate a second receptive field driven by stimuli outside the ffRF. Stimulating this feedback receptive field (fbRF) elicits slow and delayed responses compared to ffRF stimulation. These responses are preferentially reduced by anesthesia and, importantly, by silencing higher visual areas (HVAs). Feedback inputs from HVAs have scattered receptive...
A frontosensory circuit for visual context processing is synchronous in the theta/alpha band
Visual processing is strongly influenced by context. Stimuli that deviate from contextual regularities elicit augmented responses in primary visual cortex (V1). These heightened responses, known as “deviance detection,” require both inhibition local to V1 and top-down modulation from higher areas of cortex. Here we investigated the spatiotemporal mechanisms by which these circuit elements interact to support deviance detection. Local field potential recordings in mice in anterior cingulate area (ACa) and V1 during a visual oddball paradigm showed that interregional synchrony peaks in the theta/alpha band (6-12 Hz). Two-photon imaging in V1 revealed that mainly pyramidal neurons exhibited deviance detection, while vasointestinal peptide-positive interneurons (VIPs) increased activity and somatostatin-positive interneurons (SSTs) decreased activity (adapted) to redundant stimuli (prior to deviants). Optogenetic drive of ACa-V1 inputs at 6-12 Hz activated V1-VIPs but inhibited V1-SSTs,...
Contextual signals in visual cortex
Current opinion in neurobiology, 2018
Vision is an active process. What we perceive strongly depends on our actions, intentions and expectations. During visual processing, these internal signals therefore need to be integrated with the visual information from the retina. The mechanisms of how this is achieved by the visual system are still poorly understood. Advances in recording and manipulating neuronal activity in specific cell types and axonal projections together with tools for circuit tracing are beginning to shed light on the neuronal circuit mechanisms of how internal, contextual signals shape sensory representations. Here we review recent work, primarily in mice, that has advanced our understanding of these processes, focusing on contextual signals related to locomotion, behavioural relevance and predictions.
Neural mechanisms of contextual modulation in the retinal direction selective circuit
Nature Communications, 2019
Contextual modulation of neuronal responses by surrounding environments is a fundamental attribute of sensory processing. In the mammalian retina, responses of On–Off direction selective ganglion cells (DSGCs) are modulated by motion contexts. However, the underlying mechanisms are unknown. Here, we show that posterior-preferring DSGCs (pDSGCs) are sensitive to discontinuities of moving contours owing to contextually modulated cholinergic excitation from starburst amacrine cells (SACs). Using a combination of synapse-specific genetic manipulations, patch clamp electrophysiology and connectomic analysis, we identified distinct circuit motifs upstream of On and Off SACs that are required for the contextual modulation of pDSGC activity for bright and dark contrasts. Furthermore, our results reveal a class of wide-field amacrine cells (WACs) with straight, unbranching dendrites that function as “continuity detectors” of moving contours. Therefore, divergent circuit motifs in the On and ...