Short-term depression and transient memory in sensory cortex

Abstract

Persistent neuronal activity is usually studied in the context of short-term memory localized in central cortical areas. Recent studies show that early sensory areas also can have persistent representations of stimuli which emerge quickly (over tens of milliseconds) and decay slowly (over seconds). Traditional positive feedback models cannot explain sensory persistence for at least two reasons: (i) They show attractor dynamics, with transient perturbations resulting in a quasi-permanent change of system state, whereas sensory systems return to the original state after a transient. (ii) As we show, those positive feedback models which decay to baseline lose their persistence when their recurrent connections are subject to short-term depression, a common property of excitatory connections in early sensory areas. Dual time constant network behavior has also been implemented by nonlinear afferents producing a large transient input followed by much smaller steady state input. We show that such networks require unphysiologically large onset transients to produce the rise and decay observed in sensory areas. Our study explores how memory and persistence can be implemented in another model class, derivative feedback networks. We show that these networks can operate with two vastly different time courses, changing their state quickly when new information is coming in but retaining it for a long time, and that these capabilities are robust to short-term depression. Specifically, derivative feedback networks with short-term depression that acts differentially on positive and negative feedback projections are capable of dynamically changing their time constant, thus allowing fast onset and slow decay of responses without requiring unrealistically large input transients.

Nonlinear transient amplification in recurrent neural networks with short-term plasticity

“…NTA requires STP and recurrent inhibition, whose role on network dynamics have been studied in the past. Yet, STP was mainly examined in the context of stable working memory in recurrent networks (Mongillo et al, 2008; Zenke et al, 2015; Seeholzer et al, 2019) and transient delay activity following stimulus offset (Hempel et al, 2000; Gillary et al, 2017). However, its role in generating strongly amplified onset transients as a possible coding paradigm was largely ignored.…”

“…Computationally, Hebbian cell assemblies can amplify specific activity patterns through positive feedback, also referred to as Hebbian amplification. Based on these principles, several studies have shown that Hebbian amplification can drive persistent activity that outlasts a preceding stimulus (Hopfield, 1982; Amit and Brunel, 1997; Yakovlev et al, 1998; Wong and Wang, 2006; Zenke et al, 2015; Gillary et al, 2017), comparable to selective delay activity observed in the prefrontal cortex when animals are engaged in working memory tasks (Funahashi et al, 1989; Romo et al, 1999).…”

Visual cortical processing—From image to object representation

“…Grant Gillary discovered that short-term depression, which is ubiquitous among cortical neurons, can create short-term persistence in derivative feedback circuits. If short-term depression acts differentially on positive and negative feedback projections between two coupled neurons, they can change their time constant dynamically, allowing for fast onset and slow decay (Gillary et al, 2017).…”

Nonlinear transient amplification in recurrent neural networks with short-term plasticity

“…Computationally, Hebbian cell assemblies can amplify specific activity patterns through positive feedback, also referred to as Hebbian amplification. Based on these principles, several studies have shown that Hebbian amplification can drive persistent activity that outlasts a preceding stimulus ( Hopfield, 1982 ; Amit and Brunel, 1997 ; Yakovlev et al, 1998 ; Wong and Wang, 2006 ; Zenke et al, 2015 ; Gillary et al, 2017 ), comparable to selective delay activity observed in the prefrontal cortex when animals are engaged in working memory tasks ( Funahashi et al, 1989 ; Romo et al, 1999 ).…”