Temporal dynamics of energy-efficient coding in mouse primary visual cortex.

Sparse coding enables cortical populations to represent sensory inputs efficiently, yet its temporal dynamics remain poorly understood. Consistent with theoretical predictions, we show that stimulus onset triggers broad cortical activation, initially reducing sparseness and increasing mutual information. Subsequently, competitive interactions sustain mutual information as activity declines and sparseness increases.

Contrast gain control is a reparameterization of a population response curve.

Neurons in primary visual cortex (area V1) adapt in varying degrees to the average contrast of the environment, suggesting that the representation of visual stimuli may interact with the state of cortical gain control in complex ways. To investigate this possibility, we measured and analyzed the responses of neural populations in mouse V1 to visual stimuli as a function of contrast in different environments, each characterized by a unique distribution of contrast values. Our findings reveal that, for a fixed stimulus, the population response can be described by a vector function (), where the gain is a decreasing function of the mean contrast of the environment.

Contrast gain control is a reparameterization of a population response curve.

Neurons in primary visual cortex (area V1) adapt in different degrees to the average contrast of the environment, suggesting that the representation of visual stimuli may interact with the state of cortical gain control in complex ways. To investigate this possibility, we measured and analyzed the responses of neural populations to visual stimuli as a function of contrast in different environments, each characterized by a unique distribution of contrast. Our findings reveal that, for a given stimulus, the population response can be described by a vector function , where the gain is a decreasing function of the mean contrast of the environment.

On the contrast response function of adapted neural populations.

The magnitude of neural responses in sensory cortex depends on the intensity of a stimulus and its probability of being observed within the environment. How these two variables combine to influence the overall response of cortical populations remains unknown. Here we show that, in primary visual cortex, the vector magnitude of the population response is described by a separable power law that factors the intensity of a stimulus and its probability.

A power law describes the magnitude of adaptation in neural populations of primary visual cortex.

How do neural populations adapt to the time-varying statistics of sensory input? We used two-photon imaging to measure the activity of neurons in mouse primary visual cortex adapted to different sensory environments, each defined by a distinct probability distribution over a stimulus set. We find that two properties of adaptation capture how the population response to a given stimulus, viewed as a vector, changes across environments. First, the ratio between the response magnitudes is a power law of the ratio between the stimulus probabilities.

On the contrast response function of adapted neural populations.

The magnitude of neural responses in sensory cortex depends on the intensity of a stimulus and its probability of being observed within the environment. How these two variables combine to influence the overall response of cortical populations remains unknown. Here we show that, in primary visual cortex, the vector magnitude of the population response is described by a separable power-law that factors the intensity of a stimulus and its probability.

A power law of cortical adaptation.

How do neural populations adapt to the time-varying statistics of sensory input? To investigate, we measured the activity of neurons in primary visual cortex adapted to different environments, each associated with a distinct probability distribution over a stimulus set. Within each environment, a stimulus sequence was generated by independently sampling form its distribution. We find that two properties of adaptation capture how the population responses to a given stimulus, viewed as vectors, are linked across environments.

Thalamocortical boutons cluster by ON/OFF responses in mouse primary visual cortex.

In higher mammals, the thalamic afferents to primary visual cortex cluster according to their responses to increases (ON) or decreases (OFF) in luminance. This feature of thalamocortical wiring is thought to create columnar, ON/OFF domains in V1. We have recently shown that mice also have ON/OFF cortical domains, but the organization of their thalamic afferents remains unknown.

ON/OFF domains shape receptive field structure in mouse visual cortex.

In higher mammals, thalamic afferents to primary visual cortex (area V1) segregate according to their responses to increases (ON) or decreases (OFF) in luminance. This organization induces columnar, ON/OFF domains postulated to provide a scaffold for the emergence of orientation tuning. To further test this idea, we asked whether ON/OFF domains exist in mouse V1.

Vision Changes the Cellular Composition of Binocular Circuitry during the Critical Period.

High acuity stereopsis emerges during an early postnatal critical period when binocular neurons in the primary visual cortex sharpen their receptive field tuning properties. We find that this sharpening is achieved by dismantling the binocular circuit present at critical period onset and building it anew. Longitudinal imaging of receptive field tuning (e.

State-Dependent Subnetworks of Parvalbumin-Expressing Interneurons in Neocortex.

Brain state determines patterns of spiking output that underlie behavior. In neocortex, brain state is reflected in the spontaneous activity of the network, which is regulated in part by neuromodulatory input from the brain stem and by local inhibition. We find that fast-spiking, parvalbumin-expressing inhibitory neurons, which exert state-dependent control of network gain and spike patterns, cluster into two stable and functionally distinct subnetworks that are differentially engaged by ascending neuromodulation.

Local tuning biases in mouse primary visual cortex.

Neurons in primary visual cortex are selective to the orientation and spatial frequency of sinusoidal gratings. In the classic model of cortical organization, a population of neurons responding to the same region of the visual field but tuned to all possible feature combinations provides a detailed representation of the local image. Such a functional module is assumed to be replicated across primary visual cortex to provide a uniform representation of the image across the entire visual field.

On the Subspace Invariance of Population Responses.

In cat visual cortex, the response of a neural population to the linear combination of two sinusoidal gratings (a plaid) can be well approximated by a weighted sum of the population responses to the individual gratings - a property we refer to as . We tested subspace invariance in mouse primary visual cortex by measuring the angle between the population response to a plaid and the plane spanned by the population responses to its individual components. We found robust violations of subspace invariance arising from a strong, negative correlation between the responses of neurons to individual gratings and their responses to the plaid.

An inhibitory pull-push circuit in frontal cortex.

Push-pull is a canonical computation of excitatory cortical circuits. By contrast, we identify a pull-push inhibitory circuit in frontal cortex that originates in vasoactive intestinal polypeptide (VIP)-expressing interneurons. During arousal, VIP cells rapidly and directly inhibit pyramidal neurons; VIP cells also indirectly excite these pyramidal neurons via parallel disinhibition.

Pten and EphB4 regulate the establishment of perisomatic inhibition in mouse visual cortex.

Perisomatic inhibition of pyramidal neurons is established by fast-spiking, parvalbumin-expressing interneurons (PV cells). Failure to assemble adequate perisomatic inhibition is thought to underlie the aetiology of neurological dysfunction in seizures, autism spectrum disorders and schizophrenia. Here we show that in mouse visual cortex, strong perisomatic inhibition does not develop if PV cells lack a single copy of Pten.

Spatial clustering of tuning in mouse primary visual cortex.

The primary visual cortex of higher mammals is organized into two-dimensional maps, where the preference of cells for stimulus parameters is arranged regularly on the cortical surface. In contrast, the preference of neurons in the rodent appears to be arranged randomly, in what is termed a salt-and-pepper map. Here we revisited the spatial organization of receptive fields in mouse primary visual cortex by measuring the tuning of pyramidal neurons in the joint orientation and spatial frequency domain.

Enhanced Spatial Resolution During Locomotion and Heightened Attention in Mouse Primary Visual Cortex.

Unlabelled: We do not fully understand how behavioral state modulates the processing and transmission of sensory signals. Here, we studied the cortical representation of the retinal image in mice that spontaneously switched between a state of rest and a constricted pupil, and one of active locomotion and a dilated pupil, indicative of heightened attention. We measured the selectivity of neurons in primary visual cortex for orientation and spatial frequency, as well as their response gain, in these two behavioral states.

Overexpression of calcium-activated potassium channels underlies cortical dysfunction in a model of PTEN-associated autism.

De novo phosphatase and tensin homolog on chromosome ten (PTEN) mutations are a cause of sporadic autism. How single-copy loss of PTEN alters neural function is not understood. Here we report that Pten haploinsufficiency increases the expression of small-conductance calcium-activated potassium channels.

A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex.

Early sensory experience instructs the maturation of neural circuitry in the cortex. This has been studied extensively in the primary visual cortex, in which loss of vision to one eye permanently degrades cortical responsiveness to that eye, a phenomenon known as ocular dominance plasticity (ODP). Cortical inhibition mediates this process, but the precise role of specific classes of inhibitory neurons in ODP is controversial.

Associative fear learning enhances sparse network coding in primary sensory cortex.

Several models of associative learning predict that stimulus processing changes during association formation. How associative learning reconfigures neural circuits in primary sensory cortex to "learn" associative attributes of a stimulus remains unknown. Using 2-photon in vivo calcium imaging to measure responses of networks of neurons in primary somatosensory cortex, we discovered that associative fear learning, in which whisker stimulation is paired with foot shock, enhances sparse population coding and robustness of the conditional stimulus, yet decreases total network activity.

Pattern and not magnitude of neural activity determines dendritic spine stability in awake mice.

The stability of dendritic spines in the neocortex is profoundly influenced by sensory experience, which determines the magnitude and pattern of neural firing. By optically manipulating the temporal structure of neural activity in vivo using channelrhodopsin-2 and repeatedly imaging dendritic spines along these stimulated neurons over a period of weeks, we show that the specific pattern, rather than the total amount of activity, determines spine stability in awake mice.

Fast-spiking interneurons have an initial orientation bias that is lost with vision.

We found that in mice, following eye opening, fast-spiking, parvalbumin-positive GABAergic interneurons had well-defined orientation tuning preferences and that subsequent visual experience broadened this tuning. Broad inhibitory tuning was not required for the developmental sharpening of excitatory tuning but did precede binocular matching of excitatory orientation tuning. We propose that experience-dependent broadening of inhibition is a candidate for initiating the critical period of excitatory binocular plasticity in developing visual cortex.