Familiarity modulated synapses model visual cortical circuit novelty responses

Abstract

AbstractSince environments are constantly in flux, the brain’s ability to identify novel stimuli that fall outside its own internal representation of the world is crucial for an organism’s survival. Within the mammalian neocortex, inhibitory microcircuits are proposed to regulate activity in an experience-dependent manner and different inhibitory neuron subtypes exhibit distinct novelty responses. Discerning the function of diverse neural circuits and their modulation by experience can be daunting unless one has a biologically plausible mechanism to detect and learn from novel experiences that is both understandable and flexible. Here we introduce a learning mechanism,familiarity modulated synapses(FMSs), through which a network response that encodes novelty emerges from unsupervised synaptic modifications depending only on the presynaptic or both the pre- and postsynaptic activity. FMSs stand apart from other familiarity mechanisms in their simplicity: they operate under continual learning, do not require specialized architecture, and can distinguish novelty rapidly without requiring feedback. Implementing FMSs within a model of a visual cortical circuit that includes multiple inhibitory populations, we simultaneously reproduce three distinct novelty effects recently observed in experimental data from visual cortical circuits in mice: absolute, contextual, and omission novelty. Additionally, our model results in a set of diverse physiological responses across cell subpopulations, allowing us to analyze how their connectivity and synaptic dynamics influences their distinct behavior, leading to predictions that can be tested in experiment. Altogether, our findings demonstrate how experimentally-constrained cortical circuit structure can give rise to qualitatively distinct novelty responses using simple plasticity mechanisms. The flexibility of FMSs opens the door to computationally and theoretically investigating how distinct synapse modulations can lead to a variety of experience-dependent responses in a simple, understandable, and biologically plausible setup.