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Ringach, D. L.

Publications and source records attributed to Ringach, D. L..

7 recordsLinked to original sources

Adaptation shapes the representational geometry in mouse V1 to efficiently encode the environment

Sensory adaptation dynamically changes neural responses as a function of previous stimuli, profoundly impacting perception. The response changes induced by adaptation have been characterized in detail in individual neurons and at the population level after averaging across trials. However, it is not clear how adaptation modifies the aspects of the representations that relate more directly to the ability to perceive stimuli, such as their geometry and the noise structure in individual trials. To address this question, we recorded from a population of neurons in the mouse visual cortex and presented one stimulus (an oriented grating) more frequently than the others. We then analyzed these data in terms of representational geometry and studied the ability of a linear decoder to discriminate between similar visual stimuli based on the single-trial population responses. Surprisingly, the discriminability of stimuli near the adaptor increased, even though the responses of individual neurons to these stimuli decreased. This improvement arose mainly from how adaptation reshaped the geometry of the mean population responses, with changes in the noise structure playing a minor role. Locomotion modulated the population responses along a direction largely independent of adaptation, allowing the adaptation-induced increase in discriminability to persist during locomotion. Finally, artificial neural networks trained to reconstruct the visual stimulus under metabolic constraints reproduced the increase in discriminability and the decrease in responses. The paradoxical effects of adaptation are thus consistent with the efficient coding framework, allowing the brain to improve the representation of frequent stimuli while limiting the associated metabolic cost.

neuroscience↗

The development of receptive field tuning properties in mouse binocular primary visual cortex

The mouse primary visual cortex is a model system for understanding the relationship between cortical structure, function, and behavior (Seabrook et al., 2017; Chaplin and Margrie, 2020; Hooks and Chen, 2020; Saleem, 2020; Flossmann and Rochefort, 2021). Binocular neurons in V1 are the cellular basis of binocular vision, which is required for predation (Scholl et al., 2013; Hoy et al., 2016; La Chioma et al., 2020; Berson, 2021; Johnson et al., 2021). The normal development of binocular responses, however, has not been systematically measured. Here, we measure tuning properties of neurons to either eye in awake mice of either sex from eye-opening to the closure of the critical period. At eye-opening, we find an adult-like fraction of neurons responding to the contralateral-eye stimulation, which are selective for orientation and spatial frequency; few neurons respond to ipsilateral eye and their tuning is immature. Fraction of ipsilateral-eye responses increases rapidly in the first few days after eye opening and more slowly thereafter, reaching adult levels by critical period closure. Tuning of these responses improves with a similar time course. The development and tuning of binocular responses parallels that of ipsilateral-eye responses. Four days after eye-opening, monocular neurons respond to a full range of orientations but become more biased to cardinal orientations. Binocular responses, by contrast, lose their cardinal bias with age. Together, these data provide an in-depth accounting of the development of monocular and binocular responses in the binocular region of mouse V1 using a consistent set of visual stimuli and measurements. Significance statementIn this manuscript, we present a full accounting of the emergence and refinement of monocular and binocular receptive field tuning properties of thousands of pyramidal neurons in mouse primary visual cortex. Our data reveal new features of monocular and binocular development that revise current models on the emergence of cortical binocularity. Given the recent interest in visually guided behaviors in mice that require binocular vision, e.g. predation, our measures will provide the basis for studies on the emergence of the neural circuitry guiding these behaviors.

neuroscience↗

Vision is required for the formation of binocular neurons prior to the classical critical period

Depth perception emerges from the development of binocular neurons in primary visual cortex. Vision is required for these neurons to acquire their mature responses to visual stimuli. The prevailing view is that vision does not influence binocular circuitry until the onset of the critical period, about a week after eye opening, and that plasticity of visual responses is triggered by increased inhibition. Here, we show that vision is required to form binocular neurons and to improve binocular tuning and matching from eye opening until critical period closure. Enhancing inhibition does not accelerate this process. Vision soon after eye opening improves the tuning properties of binocular neurons by strengthening and sharpening ipsilateral-eye cortical responses. This progressively changes the population of neurons in the binocular pool and this plasticity is sensitive to interocular differences prior to critical period onset. Thus, vision establishes binocular circuitry and guides binocular plasticity from eye opening.

neuroscience↗

Vision reconstructs the cellular composition of binocular circuitry during the critical period

High acuity binocularity is established in primary visual cortex during an early postnatal critical period. In contrast to current models for the developmental of binocular neurons, we find that the binocular network present at the onset of the critical period is dismantled and remade. Using longitudinal imaging of receptive field tuning (e.g. orientation selectivity) of thousands of layer 2/3 neurons through development, we show most binocular neurons present at critical-period onset are poorly tuned and rendered monocular. These are replenished by newly formed binocular neurons that are established by a vision-dependent recruitment of well-tuned ipsilateral inputs to contralateral monocular neurons with matched tuning properties. The binocular network in layer 4 is equally unstable but does not improve. Thus, vision instructs a new and more sharply tuned binocular network in layer 2/3 by exchanging one population of neurons for another and not by refining an extant network. One Sentence SummaryUnstable binocular circuitry is transformed by vision into a network of highly tuned complex feature detectors in the cortex.

neuroscience↗

Functional clusters of neurons in layer 6 of macaque V1

AbstracLayer 6 appears to perform a very important role in the function of macaque primary visual cortex, V1, but not enough is understood about the functional characteristics of neurons in the layer 6 population. It is unclear to what extent the population is homogeneous with respect to their visual properties or if one can identify distinct sub-populations. Here we performed a cluster analysis based on measurements of the responses of single neurons in layer 6 of primary visual cortex to achromatic grating stimuli that varied in orientation, direction of motion, spatial and temporal frequency, and contrast. The visual stimuli were presented in a stimulus window that was also varied in size. Using the responses to parametric variation in these stimulus variables we extracted a number of tuning response measures and used them in the cluster analysis. Six main clusters emerged along with some smaller clusters. Additionally we asked whether parameter distributions from each of the clusters were statistically different. There were clear separations of parameters between some of the clusters, particularly for f1/f0 ratio, direction selectivity, and temporal frequency bandwidth but other dimensions also showed differences between clusters. Our data suggest that in layer 6, across the spatial extent of a single cortical hypercolumn, there are multiple parallel circuits that provide information about different aspects of the visual stimulus.

neuroscience↗

The Geometry of Masking in Neural Populations

We introduce a geometric approach to study the representation of orientation by populations of neurons in primary visual cortex in the presence and absence of an additive mask. Despite heterogeneous effects at the single cell level, a simple geometric model explains how population responses are transformed by the mask and reveals how changes in discriminability and bias relate to each other. We propose that studying the geometry of neural populations can yield insights into the role of contextual modulation in the processing of sensory signals.

neuroscience↗

Untangling cortical maps in mouse primary visual cortex

Local populations of neurons in mouse visual cortex exhibit diverse tuning preferences. We show this seeming disorder can be untangled -- the similarity of tuning between pairs of neurons is correlated better with the overlap between their receptive fields in visual space rather than with their distance in the cortex. These findings are consistent with the hypothesis that salt-and-pepper maps arise from the lateral dispersion of clonally related neurons.

neuroscience↗