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Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex.

ABSTRACT: The prefrontal cortex maintains information in memory through static or dynamic population codes depending on task demands, but whether the population coding schemes used are learning-dependent and differ between cell types is currently unknown. We investigate the population coding properties and temporal stability of neurons recorded from male macaques in two mapping tasks during and after stimulus-response associative learning, and then we use a Strategy task with the same stimuli and responses as control. We identify a heterogeneous population coding for stimuli, responses, and novel associations: static for putative pyramidal cells and dynamic for putative interneurons that show the strongest selectivity for all the variables. The population coding of learned associations shows overall the highest stability driven by cell types, with interneurons changing from dynamic to static coding after successful learning. The results support that prefrontal microcircuitry expresses mixed population coding governed by cell types and changes its stability during associative learning.

SUBMITTER: Ceccarelli F

PROVIDER: S-EPMC10721651 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex.

Ceccarelli Francesco F Ferrucci Lorenzo L Londei Fabrizio F Ramawat Surabhi S Brunamonti Emiliano E Genovesio Aldo A

Nature communications 20231214 1

The prefrontal cortex maintains information in memory through static or dynamic population codes depending on task demands, but whether the population coding schemes used are learning-dependent and differ between cell types is currently unknown. We investigate the population coding properties and temporal stability of neurons recorded from male macaques in two mapping tasks during and after stimulus-response associative learning, and then we use a Strategy task with the same stimuli and response ...[more]

PMID: 38097560

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Project description:Working memory (WM) provides the stability necessary for high-level cognition. Influential theories typically assume that WM depends on the persistence of stable neural representations, yet increasing evidence suggests that neural states are highly dynamic. Here we apply multivariate pattern analysis to explore the population dynamics in primate lateral prefrontal cortex (PFC) during three variants of the classic memory-guided saccade task (recorded in four animals). We observed the hallmark of dynamic population coding across key phases of a working memory task: sensory processing, memory encoding, and response execution. Throughout both these dynamic epochs and the memory delay period, however, the neural representational geometry remained stable. We identified two characteristics that jointly explain these dynamics: (1) time-varying changes in the subpopulation of neurons coding for task variables (i.e., dynamic subpopulations); and (2) time-varying selectivity within neurons (i.e., dynamic selectivity). These results indicate that even in a very simple memory-guided saccade task, PFC neurons display complex dynamics to support stable representations for WM.SIGNIFICANCE STATEMENT Flexible, intelligent behavior requires the maintenance and manipulation of incoming information over various time spans. For short time spans, this faculty is labeled "working memory" (WM). Dominant models propose that WM is maintained by stable, persistent patterns of neural activity in prefrontal cortex (PFC). However, recent evidence suggests that neural activity in PFC is dynamic, even while the contents of WM remain stably represented. Here, we explored the neural dynamics in PFC during a memory-guided saccade task. We found evidence for dynamic population coding in various task epochs, despite striking stability in the neural representational geometry of WM. Furthermore, we identified two distinct cellular mechanisms that contribute to dynamic population coding.

Dataset Information

Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex.

Publications

Static and dynamic coding in distinct cell types during associative learning in the prefrontal cortex.

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