Neural network model of the primary visual cortex: From functional architecture to lateral connectivity and back

The role of intrinsic cortical dynamics is a debatable issue. A recent optical imaging study (Kenet et al., 2003) found that activity patterns similar to orientation maps (OMs), emerge in the primary visual cortex (V1) even in the absence of sensory input, suggesting an intrinsic mechanism of OM activation. To better understand these results and shed light on the intrinsic V1 processing, we suggest a neural network model in which OMs are encoded by the intrinsic lateral connections. The proposed connectivity pattern depends on the preferred orientation and, unlike previous models, on the degree of orientation selectivity of the interconnected neurons. We prove that the network has a ring attractor composed of an approximated version of the OMs. Consequently, OMs emerge spontaneously when the network is presented with an unstructured noisy input. Simulations show that the model can be applied to experimental data and generate realistic OMs. We study a variation of the model with spatially restricted connections, and show that it gives rise to states composed of several OMs. We hypothesize that these states can represent local properties of the visual scene

Neocortical Axon Arbors Trade-off Material and Conduction Delay Conservation

The brain contains a complex network of axons rapidly communicating information between billions of synaptically connected neurons. The morphology of individual axons, therefore, defines the course of information flow within the brain. More than a century ago, Ramón y Cajal proposed that conservation laws to save material (wire) length and limit conduction delay regulate the design of individual axon arbors in cerebral cortex. Yet the spatial and temporal communication costs of single neocortical axons remain undefined. Here, using reconstructions of in vivo labelled excitatory spiny cell and inhibitory basket cell intracortical axons combined with a variety of graph optimization algorithms, we empirically investigated Cajal's conservation laws in cerebral cortex for whole three-dimensional (3D) axon arbors, to our knowledge the first study of its kind. We found intracortical axons were significantly longer than optimal. The temporal cost of cortical axons was also suboptimal though far superior to wire-minimized arbors. We discovered that cortical axon branching appears to promote a low temporal dispersion of axonal latencies and a tight relationship between cortical distance and axonal latency. In addition, inhibitory basket cell axonal latencies may occur within a much narrower temporal window than excitatory spiny cell axons, which may help boost signal detection. Thus, to optimize neuronal network communication we find that a modest excess of axonal wire is traded-off to enhance arbor temporal economy and precision. Our results offer insight into the principles of brain organization and communication in and development of grey matter, where temporal precision is a crucial prerequisite for coincidence detection, synchronization and rapid network oscillations

A Dynamic Neural Field Model of Mesoscopic Cortical Activity Captured with Voltage-Sensitive Dye Imaging

A neural field model is presented that captures the essential non-linear characteristics of activity dynamics across several millimeters of visual cortex in response to local flashed and moving stimuli. We account for physiological data obtained by voltage-sensitive dye (VSD) imaging which reports mesoscopic population activity at high spatio-temporal resolution. Stimulation included a single flashed square, a single flashed bar, the line-motion paradigm – for which psychophysical studies showed that flashing a square briefly before a bar produces sensation of illusory motion within the bar – and moving squares controls. We consider a two-layer neural field (NF) model describing an excitatory and an inhibitory layer of neurons as a coupled system of non-linear integro-differential equations. Under the assumption that the aggregated activity of both layers is reflected by VSD imaging, our phenomenological model quantitatively accounts for the observed spatio-temporal activity patterns. Moreover, the model generalizes to novel similar stimuli as it matches activity evoked by moving squares of different speeds. Our results indicate that feedback from higher brain areas is not required to produce motion patterns in the case of the illusory line-motion paradigm. Physiological interpretation of the model suggests that a considerable fraction of the VSD signal may be due to inhibitory activity, supporting the notion that balanced intra-layer cortical interactions between inhibitory and excitatory populations play a major role in shaping dynamic stimulus representations in the early visual cortex

Predicted contextual modulation varies with distance from pinwheel centers in the orientation preference map

In the primary visual cortex (V1) of some mammals, columns of neurons with the full range of orientation preferences converge at the center of a pinwheel-like arrangement, the ‘pinwheel center' (PWC). Because a neuron receives abundant inputs from nearby neurons, the neuron's position on the cortical map likely has a significant impact on its responses to the layout of orientations inside and outside its classical receptive field (CRF). To understand the positional specificity of responses, we constructed a computational model based on orientation preference maps in monkey V1 and hypothetical neuronal connections. The model simulations showed that neurons near PWCs displayed weaker but detectable orientation selectivity within their CRFs, and strongly reduced contextual modulation from extra-CRF stimuli, than neurons distant from PWCs. We suggest that neurons near PWCs robustly extract local orientation within their CRF embedded in visual scenes, and that contextual information is processed in regions distant from PWCs

Neuron-glial Interactions

Although lagging behind classical computational neuroscience, theoretical and computational approaches are beginning to emerge to characterize different aspects of neuron-glial interactions. This chapter aims to provide essential knowledge on neuron-glial interactions in the mammalian brain, leveraging on computational studies that focus on structure (anatomy) and function (physiology) of such interactions in the healthy brain. Although our understanding of the need of neuron-glial interactions in the brain is still at its infancy, being mostly based on predictions that await for experimental validation, simple general modeling arguments borrowed from control theory are introduced to support the importance of including such interactions in traditional neuron-based modeling paradigms.Junior Leader Fellowship Program by “la Caixa” Banking Foundation (LCF/BQ/LI18/11630006

Neuron-Glial Interactions

Although lagging behind classical computational neuroscience, theoretical and computational approaches are beginning to emerge to characterize different aspects of neuron-glial interactions. This chapter aims to provide essential knowledge on neuron-glial interactions in the mammalian brain, leveraging on computational studies that focus on structure (anatomy) and function (physiology) of such interactions in the healthy brain. Although our understanding of the need of neuron-glial interactions in the brain is still at its infancy, being mostly based on predictions that await for experimental validation, simple general modeling arguments borrowed from control theory are introduced to support the importance of including such interactions in traditional neuron-based modeling paradigms.Comment: 43 pages, 2 figures, 1 table. Accepted for publication in the "Encyclopedia of Computational Neuroscience," D. Jaeger and R. Jung eds., Springer-Verlag New York, 2020 (2nd edition

The relationship between GABA immunoreactivity and labelling by local uptake of [3H]GABA in the striate cortex of monkey.

An antiserum to GABA was used in the macaque monkey to determine whether neurons that accumulate exogenously applied [3H]GABA in vivo are also immunoreactive for GABA. Following the injection of [3H]GABA into different laminae of striate cortex in two untreated animals and in one animal treated with amino-oxyacetic acid, selective accumulation of the labelled amino acid was demonstrated in perikarya by autoradiography. Radiographically labelled neurons (n, 519) and their unlabelled neighbours were tested in consecutive 0.5 micron thick sections by immunocytochemistry for GABA immunoreactivity. Injection of [3H]GABA did not increase the number of neurons showing GABA immunoreactivity. On the contrary many of the cells that accumulated [3H]GABA were immunonegative. These neurons were mostly located in layers IVC and VA following [3H]GABA injection into layers II-III, and in layers upper III and II following injection into layers V and VI. A comparison of the position of these neurons with known local projection patterns in the striate cortex of monkey suggests that GABA-immunonegative neurons may nevertheless become labelled by [3H]GABA if most of their local axon terminals fall within the injection site. The interlaminar projection of GABA-immunopositive neurons, which probably contain endogenous GABA, could be deduced from the position of the [3H]GABA injection site that leads to their autoradiographic labelling. Although the present study confirmed our previous results on the interlaminar connections of neurons that accumulate [3H]GABA, it demonstrated that [3H]GABA labelling alone may not be a sufficient criterion to assess the GABAergic nature of neurons in the striate cortex of monkey

Characterization by Golgi impregnation of neurons that accumulate 3H-GABA in the visual cortex of monkey.

3H-GABA was injected into restricted regions of visual areas 1 and 2 (cortical areas 17 and 18) on the lateral surface of the occipital lobe in monkeys. The injected tissue was processed for Golgi impregnation and gold toning. Sections containing Golgi-impregnated neurons were re-embedded, sectioned at 1 micron, and prepared for autoradiography to reveal neurones that had selectively accumulated 3H-GABA. Golgi-impregnated pyramidal, spiny stellate and aspiny nonpyramidal neurons were examined for 3H-GABA accumulation. Out of 47 aspiny non-pyramidal neurons 16 were labelled by 3H-GABA. The other cell types did not accumulate the amino acid. Twelve of the labelled neurons were drawn. Eight were bitufted neurons with their dendrites oriented predominantly radially, three were small multipolar neurons, and one could be reconstructed only partially. One neuron had a locally arborizing axon in layer III. Two bitufted, Golgi-impregnated neurons in layer II and upper III of area 18 were labelled from GABA injection radially beneath in layer VI, providing evidence for earlier suggestions that in the monkey's visual cortex the cells in the upper layers which project radially and accumulate 3H-GABA are aspiny non-pyramidal cells. The results indicate the existence of different types of putative GABA-ergic interneurons