Abstract
Competitive interactions are believed to underlie many types of cortical processing, ranging from memory formation, attention and development of cortical functional organization (e.g., development of orientation maps in primary visual cortex). In the latter case, the competitive interactions happen along the cortical surface, with local populations of neurons reinforcing each other, while competing with those displaced more distally. This specific configuration of lateral interactions is however in stark contrast with the known properties of the anatomical substrate, i.e., excitatory connections (mediating reinforcement) having longer reach than inhibitory ones (mediating competition). No satisfactory biologically plausible resolution of this conflict between anatomical measures, and assumed cortical function has been proposed. Recently a specific pattern of delays between different types of neurons in cat cortex has been discovered, where direct mono-synaptic excitation has approximately the same delay, as the combined delays of the disynaptic inhibitory interactions between excitatory neurons (i.e., the sum of delays from excitatory to inhibitory and from inhibitory to excitatory neurons). Here we show that this specific pattern of delays represents a biologically plausible explanation for how short-range inhibition can support competitive interactions that underlie the development of orientation maps in primary visual cortex. We demonstrate this statement analytically under simplifying conditions, and subsequently show using network simulations that development of orientation maps is preserved when long-range excitation, direct inhibitory to inhibitory interactions, and moderate inequality in the delays between excitatory and inhibitory pathways is added.
Highlights
Competition between populations of neurons has been proposed as one of the canonical computations of cortical networks, and has been hypothesized to underly a range of brain functions including working memory (Amit and Brunel, 1995; Durstewitz et al, 2000), orientation tuning (Ben-Yishai et al, 1995; Somers et al, 1995), and functional map development
In this study we explore the possibility that this specific transmission delay pattern is the missing link that can explain how short range inhibition can lead to effective cortical competition
Several mechanistic explanations of how orientation maps can develop in primary visual cortex have been proposed, but most, including the LISSOM family of models, involve two key ingredients: (1) stimulus driven Hebbian learning on the thalamo-cortical synapses, that ensures the formation of afferent connectivity pattern inducing Gabor like RFs to V1 neural units; and (2) a Mexican-hat-like effective lateral interactions within the cortical population of neural units, that induce co-activation among proximate units while competition between more distal units
Summary
Competition between populations of neurons has been proposed as one of the canonical computations of cortical networks, and has been hypothesized to underly a range of brain functions including working memory (Amit and Brunel, 1995; Durstewitz et al, 2000), orientation tuning (Ben-Yishai et al, 1995; Somers et al, 1995), and functional map development (von der Malsburg, 1973; Miikkulainen et al, 2005; Antolík and Bednar, 2011). This explanation has never been explicitly demonstrated, and it omits the fact that under the reasonable null-hypothesis of equal transmission delays for all connections, the recurrent disynaptic inhibition will lag the direct recurrent excitation As it turns out this is crucial, as recent model analysis by Muir et al (Muir and Cook, 2014) shows that, under the assumption of uniform transmission delays, the presence of competition across the cortical surface is predicted well by the anatomy of direct excitatory and inhibitory coupling and that multi-synaptic network effects are negligible, effectively rejecting the disynaptic explanation behind Maxican-hat interaction. Currently no satisfactory explanation of how topological functional organization develops in cortical networks that is consistent with the present anatomical findings exists
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