Between persistently active and activity‐silent frameworks: novel vistas on the cellular basis of working memory

Abstract

Recent work has revealed important new discoveries on the cellular mechanisms of working memory (WM). These findings have motivated several seemingly conflicting theories on the mechanisms of short‐term memory maintenance. Here, we summarize the key insights gained from these new experiments and critically evaluate them in light of three hypotheses: classical persistent activity, activity‐silent, and dynamic coding. The experiments discussed include the first direct demonstration of persistently active neurons in the human medial temporal lobe that form static attractors with relevance to WM, single‐neuron recordings in the macaque prefrontal cortex that show evidence for both persistent and more dynamic types of WM representations, and noninvasive neuroimaging in humans that argues for activity‐silent representations. A key insight that emerges from these new results is that there are several neural mechanisms that support the maintenance of information in WM. Finally, based on established cognitive theories of WM, we propose a coherent model that encompasses these seemingly contradictory results. We propose that the three neuronal mechanisms of persistent activity, activity‐silent, and dynamic coding map well onto the cognitive levels of information processing (within focus of attention, activated long‐term memory, and central executive) that Cowan's WM model proposes.

Theoretical distinction between functional states in working memory and their corresponding neural states

“…Finally, we consider the proposal that functionally active states are supported by elevated neural activity, whereas functionally latent states correspond to activity-silent mnemonic mechanisms. This distinction has been suggested by a number of authors (e.g., Kamiński & Rutishauser, 2019;LaRocque et al, 2013LaRocque et al, , 2015Lewis-Peacock et al, 2012;Manohar et al, 2019;Olivers et al, 2011;Stokes, 2015). In the framework developed here, this division of labour is only helpful if it confers differential functional properties on active and latent WMs.…”

Neuronal firing in the medial temporal lobe reflects human working memory workload, performance and capacity

“…Updating and maintaining working memory content requires collaboration between multiple areas in the brain. Core neural structures are located in the posterior parietal cortex and prefrontal cortex, while the role of the MTL is unclear (for reviews see (5, 6)). The posterior parietal cortex supports elementary functions that are necessary for multiple object maintenance.…”

“…Electrophysiology and neuroimaging evidence specifically links MTL activity to maintenance in working memory. A recent review on single neuron recordings suggested direct involvement of MTL neural firing patterns in working memory (6). Patterns of neural activity were consistent to specific predictions from Cowan’s activated long-term memory model of working memory.…”

H-Mem: Harnessing synaptic plasticity with Hebbian Memory Networks

“…Several models have been proposed for the implementation of working memory capabilities in neural networks. They have been divided into three categories: classical persistent activity, activity silent, and dynamic coding [13]. While models based on persistent activity do not engage any synaptic plasticity mechanism [14], activity-silent models and some dynamic coding models exploit short-term synaptic plasticity or neuronal adaptation [15]- [17].…”