Recurrent circuit dynamics underlie persistent activity in the macaque frontoparietal network.

Eric Hart,Alexander C Huk

doi:10.7554/elife.52460

Abstract

During delayed oculomotor response tasks, neurons in the lateral intraparietal area (LIP) and the frontal eye fields (FEF) exhibit persistent activity that reflects the active maintenance of behaviorally relevant information. Despite many computational models of the mechanisms of persistent activity, there is a lack of circuit-level data from the primate to inform the theories. To fill this gap, we simultaneously recorded ensembles of neurons in both LIP and FEF while macaques performed a memory-guided saccade task. A population encoding model revealed strong and symmetric long-timescale recurrent excitation between LIP and FEF. Unexpectedly, LIP exhibited stronger local functional connectivity than FEF, and many neurons in LIP had longer network and intrinsic timescales. The differences in connectivity could be explained by the strength of recurrent dynamics in attractor networks. These findings reveal reciprocal multi-area circuit dynamics in the frontoparietal network during persistent activity and lay the groundwork for quantitative comparisons to theoretical models.

Highlights

IntroductionPersistent neural activity is prevalent in many cortical and subcortical areas (Andersen et al, 1987; Bruce and Goldberg, 1985; Constantinidis and Steinmetz, 1996; Fuster and Alexander, 1971; Fuster and Jervey, 1981; Bolkan et al, 2017; Ferraina et al, 2002; Guo et al, 2017; Inagaki et al, 2019; Mays and Sparks, 1980; Schmitt et al, 2017), and has been studied extensively in the context of delayed oculomotor response tasks (Funahashi et al, 1989; Gnadt and Andersen, 1988; Hikosaka and Wurtz, 1983)
In order to test whether recurrent functional interactions in the frontoparietal network underlie persistent activity, we recorded ensembles of neurons (~5–20 cells per session) in areas lateral intraparietal area (LIP) and frontal eye fields (FEF) simultaneously (Figure 1a; 967 units, LIP: 407; FEF: 560; 7448 pairs)
We characterized the interneuronal interactions in this circuit during oculomotor working memory using multi-area multi-site simultaneous recordings, and a population encoding framework that extended the generalized linear model to simultaneous fits of multiple neurons recorded at the same time in two cortical areas

Summary

Introduction

Persistent neural activity is prevalent in many cortical and subcortical areas (Andersen et al, 1987; Bruce and Goldberg, 1985; Constantinidis and Steinmetz, 1996; Fuster and Alexander, 1971; Fuster and Jervey, 1981; Bolkan et al, 2017; Ferraina et al, 2002; Guo et al, 2017; Inagaki et al, 2019; Mays and Sparks, 1980; Schmitt et al, 2017), and has been studied extensively in the context of delayed oculomotor response tasks (Funahashi et al, 1989; Gnadt and Andersen, 1988; Hikosaka and Wurtz, 1983). Because persistent activity lasts far longer than the intrinsic cellular time constants of most neurons, theoretical models of persistent activity have focused on how a mix of circuit and cellular mechanisms might interact to transcend the timescale of individual neurons These models rely on a core architecture that includes recurrent excitatory connectivity, balanced inhibition, and a subset of single neurons with long (but realistic) intrinsic time constants (Amit and Brunel, 1997; Compte, 2006; Compte et al, 2000; Tegner et al, 2002; Wang, 1999; Wang, 2001). These models are remarkable for using biologically plausible elements to show how the brain could in theory exhibit persistent activity at an aggregate level, little is known about the detailed patterns of circuit-scale spiking activity in the primate brain areas that originally motivated these theories

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Results

Conclusion