Frontotemporal coordination predicts working memory performance and its local neural signatures

Ehsan Rezayat,Mohammad-Reza A Dehaqani,Zahra Bahmani,Kelsey Clark,Tirin Moore,Behrad Noudoost

doi:10.1038/s41467-021-21151-1

Abstract

Neurons in some sensory areas reflect the content of working memory (WM) in their spiking activity. However, this spiking activity is seldom related to behavioral performance. We studied the responses of inferotemporal (IT) neurons, which exhibit object-selective activity, along with Frontal Eye Field (FEF) neurons, which exhibit spatially selective activity, during the delay period of an object WM task. Unlike the spiking activity and local field potentials (LFPs) within these areas, which were poor predictors of behavioral performance, the phase-locking of IT spikes and LFPs with the beta band of FEF LFPs robustly predicted successful WM maintenance. In addition, IT neurons exhibited greater object-selective persistent activity when their spikes were locked to the phase of FEF LFPs. These results reveal that the coordination between prefrontal and temporal cortex predicts the successful maintenance of visual information during WM.

Highlights

Neurons in some sensory areas reflect the content of working memory (WM) in their spiking activity
To examine the neural basis of object WM, we trained two monkeys to perform an object delayed-match-to-sample (DMS) task (Fig. 1a) in which they had to remember the identity of a sample stimulus throughout a delay period (1 s)
Since neither spiking nor local field potentials (LFPs) activity within Frontal Eye Field (FEF) or IT was strongly predictive of performance, we investigated the synchronization between FEF and IT sites in our search for behavioral correlates of WM

Summary

Introduction

Neurons in some sensory areas reflect the content of working memory (WM) in their spiking activity. Such models involve interactions between PFC and sensory areas during memory maintenance Variations of this idea range from a more modular perspective, in which specific portions of PFC exhibiting memory activity send that signal to sensory areas[5,6], or a split of abstract vs detailed information[7] (perhaps varying based on task demands8), to more distributed versions emphasizing the content-specific communication between areas rather than spiking activity within either[9]. These conceptual models are not necessarily mutually exclusive, but they all predict that memory-related activity in sensory areas should be related to WM performance, a prediction that is discrepant with much of the existing neural data.

Methods

Results

Conclusion