Search

Summary: Correlated variability in the visual cortex is modulated by stimulus properties. The stimulus dependence of correlated variability impacts stimulus coding and is indicative of circuit structure. An affine model combining a multiplicative factor and an additive offset has been proposed to explain how correlated variability in primary visual cortex (V1) depends on stimulus orientations. However, whether the affine model could be extended to explain modulations by other stimulus variables or variability shared between two brain areas is unknown. Motivated by a simple neural circuit mechanism, we modified the affine model to better explain the contrast dependence of neural variability shared within either primary or secondary visual cortex (V1 or V2) as well as the orientation dependence of neural variability shared between V1 and V2. Our results bridge neural circuit mechanisms and statistical models and provide a parsimonious explanation for the stimulus dependence of correlated variability within and between visual areas.

For the brain to recognize local orientations within images, neurons must spontaneously break the translation and rotation symmetry of their response functions—an archetypal example of unsupervised learning. The dominant framework for unsupervised learning in biology is Hebb’s principle, but how Hebbian learning could break such symmetries is a longstanding biophysical riddle. Theoretical studies argue that this requires inputs to the visual cortex to invert the relative magnitude of their correlations at long distances. Empirical measurements have searched in vain for such an inversion and report the opposite to be true. We formally approach the question through the Hermitianization of a multilayer model, which maps it into a problem of zero-temperature phase transitions. In the emerging phase diagram, both symmetries break spontaneously as long as (i) recurrent interactions are sufficiently long range and (ii) Hebbian competition is duly accounted for. A key ingredient for symmetry breaking is competition among connections sprouting from the same afferent cell. Such a competition, along with simple monotonic falloff of input correlations with distance, is capable of triggering the broken-symmetry phase required by image processing. We provide analytic predictions on the relative magnitudes of the relevant length scales needed for this novel mechanism to occur. These results reconcile experimental observations to the Hebbian paradigm, shed light on a new mechanism for visual cortex development, and contribute to our growing understanding of the relationship between learning and symmetry breaking.

A cornerstone of theoretical neuroscience is the circuit model: a system of equations that captures a hypothesized neural mechanism. Such models are valuable when they give rise to an experimentally observed phenomenon -- whether behavioral or a pattern of neural activity -- and thus can offer insights into neural computation. The operation of these circuits, like all models, critically depends on the choice of model parameters. A key step is then to identify the model parameters consistent with observed phenomena: to solve the inverse problem. In this work, we present a novel technique, emergent property inference (EPI), that brings the modern probabilistic modeling toolkit to theoretical neuroscience. When theorizing circuit models, theoreticians predominantly focus on reproducing computational properties rather than a particular dataset. Our method uses deep neural networks to learn parameter distributions with these computational properties. This methodology is introduced through a motivational example of parameter inference in the stomatogastric ganglion. EPI is then shown to allow precise control over the behavior of inferred parameters and to scale in parameter dimension better than alternative techniques. In the remainder of this work, we present novel theoretical findings in models of primary visual cortex and superior colliculus, which were gained through the examination of complex parametric structure captured by EPI. Beyond its scientific contribution, this work illustrates the variety of analyses possible once deep learning is harnessed towards solving theoretical inverse problems.

How does attentional modulation of neural activity enhance performance? Here we use a deep convolutional neural network as a large-scale model of the visual system to address this question. We model the feature similarity gain model of attention, in which attentional modulation is applied according to neural stimulus tuning. Using a variety of visual tasks, we show that neural modulations of the kind and magnitude observed experimentally lead to performance changes of the kind and magnitude observed experimentally. We find that, at earlier layers, attention applied according to tuning does not successfully propagate through the network, and has a weaker impact on performance than attention applied according to values computed for optimally modulating higher areas. This raises the question of whether biological attention might be applied at least in part to optimize function rather than strictly according to tuning. We suggest a simple experiment to distinguish these alternatives.

When stimulated, neural populations in the visual cortex exhibit fast rhythmic activity with frequencies in the gamma band (30-80 Hz). The gamma rhythm manifests as a broad resonance peak in the power-spectrum of recorded local field potentials, which exhibits various stimulus dependencies. In particular, in macaque primary visual cortex (V1), the gamma peak frequency increases with increasing stimulus contrast. Moreover, this contrast dependence is local: when contrast varies smoothly over visual space, the gamma peak frequency in each cortical column is controlled by the local contrast in that column's receptive field. No parsimonious mechanistic explanation for these contrast dependencies of V1 gamma oscillations has been proposed. The stabilized supralinear network (SSN) is a mechanistic model of cortical circuits that has accounted for a range of visual cortical response nonlinearities and contextual modulations, as well as their contrast dependence. Here, we begin by showing that a reduced SSN model without retinotopy robustly captures the contrast dependence of gamma peak frequency, and provides a mechanistic explanation for this effect based on the observed non-saturating and supralinear input-output function of V1 neurons. Given this result, the local dependence on contrast can trivially be captured in a retinotopic SSN which however lacks horizontal synaptic connections between its cortical columns. However, long-range horizontal connections in V1 are in fact strong, and underlie contextual modulation effects such as surround suppression. We thus explored whether a retinotopically organized SSN model of V1 with strong excitatory horizontal connections can exhibit both surround suppression and the local contrast dependence of gamma peak frequency. We found that retinotopic SSNs can account for both effects, but only when the horizontal excitatory projections are composed of two components with different patterns of spatial fall-off with distance: a short-range component that only targets the source column, combined with a long-range component that targets columns neighboring the source column. We thus make a specific qualitative prediction for the spatial structure of horizontal connections in macaque V1, consistent with the columnar structure of cortex.

We examine the effects of short-term synaptic depression on the orientation tuning of the LGN input to simple cells in cat primary visual cortex (V1). The total LGN input has an untuned component as well as a tuned component, both of which grow with stimulus contrast. The untuned component is not visible in the firing rate responses of the simple cells. The suppression of the contribution of the untuned input component to firing rate responses is key to establishing orientation selectivity and its invariance with stimulus contrast. It has been argued that synaptic depression of LGN inputs could contribute to the selective suppression of the untuned component and thus contribute to the tuning observed in simple cells. We examine this using a model fit to the depression observed at thalamocortical synapses in-vivo, and compare this to an earlier model fit based on in-vitro observations. We examine the tuning of both the conductance and the firing rate induced in simple cells by the net LGN input. We find that depression causes minimal suppression of the untuned component. The primary effect of depression is to cause the contrast response curve to saturate at lower contrasts without differentially affecting the tuned vs. untuned components. This effect is slightly weaker for in-vivo vs. in-vitro parameters. Thus, synaptic depression of LGN inputs does not appreciably contribute to the orientation tuning of V1 simple cells.