Emergence of Functional Specificity in Balanced Networks with Synaptic Plasticity

Abstract

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.

Author Summary

In primary visual cortex of mammals, neurons are selective to the orientation of contrast edges. In some species, as cats and monkeys, neurons preferring similar orientations are adjacent on the cortical surface, leading to smooth orientation maps. In rodents, in contrast, such spatial orientation maps do not exist, and neurons of different specificities are mixed in a salt-and-pepper fashion. During development, however, a “functional” map of orientation selectivity emerges, where connections between neurons of similar preferred orientations are selectively enhanced. Here we show how such feature-specific connectivity can arise in realistic neocortical networks of excitatory and inhibitory neurons. Our results demonstrate how recurrent dynamics can work in cooperation with synaptic plasticity to form networks where neurons preferring similar stimulus features connect more strongly together. Such networks, in turn, are known to enhance the specificity of neuronal responses to a stimulus. Our study thus reveals how self-organizing connectivity in neuronal networks enable them to achieve new or enhanced functions, and it underlines the essential role of recurrent inhibition and plasticity in this process.