Emergent Orientation Selectivity from Random Networks in Mouse Visual Cortex

The connectivity principles underlying the emergence of orientation selectivity in primary visual cortex (V1) of mammals lacking an orientation map (such as rodents and lagomorphs) are poorly understood. We present a computational model in which random connectivity gives rise to orientation selectivity that matches experimental observations. The model predicts that mouse V1 neurons should exhibit intricate receptive fields in the two-dimensional frequency domain, causing a shift in orientation preferences with spatial frequency. We find evidence for these features in mouse V1 using calcium imaging and intracellular whole-cell recordings. Pattadkal et al. show that orientation selectivity can emerge from random connectivity, and offer a distinct perspective for how computations occur in the neocortex. They propose that a random convergence of inputs can provide signals for orientation preference in contrast with the dominant model that requires a precise arrangement.Fil: Pattadkal, Jagruti J.. University of Texas at Austin; Estados UnidosFil: Mato, German. Comisión Nacional de Energía Atómica. Gerencia del Área de Energía Nuclear. Instituto Balseiro; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: van Vreeswijk, Carl. Centre National de la Recherche Scientifique; FranciaFil: Priebe, Nicholas J.. University of Texas at Austin; Estados UnidosFil: Hansel, David. Centre National de la Recherche Scientifique; Franci

Neural population coding: combining insights from microscopic and mass signals

Behavior relies on the distributed and coordinated activity of neural populations. Population activity can be measured using multi-neuron recordings and neuroimaging. Neural recordings reveal how the heterogeneity, sparseness, timing, and correlation of population activity shape information processing in local networks, whereas neuroimaging shows how long-range coupling and brain states impact on local activity and perception. To obtain an integrated perspective on neural information processing we need to combine knowledge from both levels of investigation. We review recent progress of how neural recordings, neuroimaging, and computational approaches begin to elucidate how interactions between local neural population activity and large-scale dynamics shape the structure and coding capacity of local information representations, make them state-dependent, and control distributed populations that collectively shape behavior

Nonlinear Hebbian learning as a unifying principle in receptive field formation

The development of sensory receptive fields has been modeled in the past by a variety of models including normative models such as sparse coding or independent component analysis and bottom-up models such as spike-timing dependent plasticity or the Bienenstock-Cooper-Munro model of synaptic plasticity. Here we show that the above variety of approaches can all be unified into a single common principle, namely Nonlinear Hebbian Learning. When Nonlinear Hebbian Learning is applied to natural images, receptive field shapes were strongly constrained by the input statistics and preprocessing, but exhibited only modest variation across different choices of nonlinearities in neuron models or synaptic plasticity rules. Neither overcompleteness nor sparse network activity are necessary for the development of localized receptive fields. The analysis of alternative sensory modalities such as auditory models or V2 development lead to the same conclusions. In all examples, receptive fields can be predicted a priori by reformulating an abstract model as nonlinear Hebbian learning. Thus nonlinear Hebbian learning and natural statistics can account for many aspects of receptive field formation across models and sensory modalities

Computing motion in the primate's visual system

Computing motion on the basis of the time-varying image intensity is a difficult problem for both artificial and biological vision systems. We will show how one well-known gradient-based computer algorithm for estimating visual motion can be implemented within the primate's visual system. This relaxation algorithm computes the optical flow field by minimizing a variational functional of a form commonly encountered in early vision, and is performed in two steps. In the first stage, local motion is computed, while in the second stage spatial integration occurs. Neurons in the second stage represent the optical flow field via a population-coding scheme, such that the vector sum of all neurons at each location codes for the direction and magnitude of the velocity at that location. The resulting network maps onto the magnocellular pathway of the primate visual system, in particular onto cells in the primary visual cortex (V1) as well as onto cells in the middle temporal area (MT). Our algorithm mimics a number of psychophysical phenomena and illusions (perception of coherent plaids, motion capture, motion coherence) as well as electrophysiological recordings. Thus, a single unifying principle ‘the final optical flow should be as smooth as possible’ (except at isolated motion discontinuities) explains a large number of phenomena and links single-cell behavior with perception and computational theory

State Dependence of Stimulus-Induced Variability Tuning in Macaque MT

Behavioral states marked by varying levels of arousal and attention modulate some properties of cortical responses (e.g. average firing rates or pairwise correlations), yet it is not fully understood what drives these response changes and how they might affect downstream stimulus decoding. Here we show that changes in state modulate the tuning of response variance-to-mean ratios (Fano factors) in a fashion that is neither predicted by a Poisson spiking model nor changes in the mean firing rate, with a substantial effect on stimulus discriminability. We recorded motion-sensitive neurons in middle temporal cortex (MT) in two states: alert fixation and light, opioid anesthesia. Anesthesia tended to lower average spike counts, without decreasing trial-to-trial variability compared to the alert state. Under anesthesia, within-trial fluctuations in excitability were correlated over longer time scales compared to the alert state, creating supra-Poisson Fano factors. In contrast, alert-state MT neurons have higher mean firing rates and largely sub-Poisson variability that is stimulus-dependent and cannot be explained by firing rate differences alone. The absence of such stimulus-induced variability tuning in the anesthetized state suggests different sources of variability between states. A simple model explains state-dependent shifts in the distribution of observed Fano factors via a suppression in the variance of gain fluctuations in the alert state. A population model with stimulus-induced variability tuning and behaviorally constrained information-limiting correlations explores the potential enhancement in stimulus discriminability by the cortical population in the alert state.Comment: 36 pages, 18 figure

Modeling the Possible Influences of Eye Movements on the Refinement of Cortical Direction Selectivity

The second-order statistics of neural activity was examined in a model of the cat LGN and V1 during free-viewing of natural images. In the model, the specific patterns of thalamocortical activity required for a Bebbian maturation of direction-selective cells in VI were found during the periods of visual fixation, when small eye movements occurred, but not when natural images were examined in the absence of fixational eye movements. In addition, simulations of stroboscopic reming that replicated the abnormal pattern of eye movements observed in kittens chronically exposed to stroboscopic illumination produced results consistent with the reported loss of direction selectivity and preservation of orientation selectivity. These results suggest the involvement of the oculomotor activity of visual fixation in the maturation of cortical direction selectivity

Motion clouds: model-based stimulus synthesis of natural-like random textures for the study of motion perception

Choosing an appropriate set of stimuli is essential to characterize the response of a sensory system to a particular functional dimension, such as the eye movement following the motion of a visual scene. Here, we describe a framework to generate random texture movies with controlled information content, i.e., Motion Clouds. These stimuli are defined using a generative model that is based on controlled experimental parametrization. We show that Motion Clouds correspond to dense mixing of localized moving gratings with random positions. Their global envelope is similar to natural-like stimulation with an approximate full-field translation corresponding to a retinal slip. We describe the construction of these stimuli mathematically and propose an open-source Python-based implementation. Examples of the use of this framework are shown. We also propose extensions to other modalities such as color vision, touch, and audition

Deciphering the brain's codes

The two sensory systems discussed use similar algorithms for the synthesis of the neuronal selectivity for the stimulus that releases a particular behavior, although the neural circuits, the brain sites involved, and even the species are different. This stimulus selectivity emerges gradually in a neural network organized according to parallel and hierarchical design principles. The parallel channels contain lower order stations with special circuits for the creation of neuronal selectivities for different features of the stimulus. Convergence of the parallel pathways brings these selectivities together at a higher order station for the eventual synthesis of the selectivity for the whole stimulus pattern. The neurons that are selective for the stimulus are at the top of the hierarchy, and they form the interface between the sensory and motor systems or between sensory systems of different modalities. The similarities of these two systems at the level of algorithms suggest the existence of rules of signal processing that transcend different sensory systems and species of animals

Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity

In rodent visual cortex, synaptic connections between orientation-selective neurons are unspecific at the time of eye opening, and become to some degree functionally specific only later during development. An explanation for this two-stage process was proposed in terms of Hebbian plasticity based on visual experience that would eventually enhance connections between neurons with similar response features. For this to work, however, two conditions must be satisfied: First, orientation selective neuronal responses must exist before specific recurrent synaptic connections can be established. Second, Hebbian learning must be compatible with the recurrent network dynamics contributing to orientation selectivity, and the resulting specific connectivity must remain stable for unspecific background activity. Previous studies have mainly focused on very simple models, where the receptive fields of neurons were essentially determined by feedforward mechanisms, and where the recurrent network was small, lacking the complex recurrent dynamics of large-scale networks of excitatory and inhibitory neurons. Here we studied the emergence of functionally specific connectivity in large-scale recurrent networks with synaptic plasticity. Our results show that balanced random networks, which already exhibit highly selective responses at eye opening, can develop feature-specific connectivity if appropriate rules of synaptic plasticity are invoked within and between excitatory and inhibitory populations. If these conditions are met, the initial orientation selectivity guides the process of Hebbian learning and, as a result, functionally specific and a surplus of bidirectional connections emerge. Our results thus demonstrate the cooperation of synaptic plasticity and recurrent dynamics in large-scale functional networks with realistic receptive fields, highlight the role of inhibition as a critical element in this process, and paves the road for further computational studies of sensory processing in neocortical network models equipped with synaptic plasticity