Complementary Inhibitory Weight Profiles Emerge from Plasticity and Allow Flexible Switching of Receptive Fields

Abstract

Cortical areas comprise multiple types of inhibitory interneurons, with stereotypical connectivity motifs that may follow specific plasticity rules. Yet, their combined effect on postsynaptic dynamics has been largely unexplored. Here, we analyze the response of a single postsynaptic model neuron receiving tuned excitatory connections alongside inhibition from two plastic populations. Synapses from each inhibitory population change according to distinct plasticity rules. We tested different combinations of three rules: Hebbian, anti-Hebbian, and homeostatic scaling. Depending on the inhibitory plasticity rule, synapses become unspecific (flat), anticorrelated to, or correlated with excitatory synapses. Crucially, the neuron's receptive field (i.e., its response to presynaptic stimuli) depends on the modulatory state of inhibition. When both inhibitory populations are active, inhibition balances excitation, resulting in uncorrelated postsynaptic responses regardless of the inhibitory tuning profiles. Modulating the activity of a given inhibitory population produces strong correlations to either preferred or nonpreferred inputs, in line with recent experimental findings that show dramatic context-dependent changes of neurons' receptive fields. We thus confirm that a neuron's receptive field does not follow directly from the weight profiles of its presynaptic afferents. Our results show how plasticity rules in various cell types can interact to shape cortical circuit motifs and their dynamics.

SIGNIFICANCE STATEMENT Neurons in sensory areas of the cortex are known to respond to specific features of a given input (e.g., specific sound frequencies), but recent experimental studies show that such responses (i.e., their receptive fields) depend on context. Inspired by the cortical connectivity, we built models of excitatory and inhibitory inputs onto a single neuron, to study how receptive fields may change on short and long time scales. We show how various synaptic plasticity rules allow for the emergence of diverse connectivity profiles and, moreover, how their dynamic interaction creates a mechanism by which postsynaptic responses can quickly change. Our work emphasizes multiple roles of inhibition in cortical processing and provides a first mechanistic model for flexible receptive fields.