Distinct Spiking Patterns of Excitatory and Inhibitory Neurons and LFP Oscillations in Prefrontal Cortex During Sensory Discrimination.

Hua-An Tseng,Xue Han

doi:10.3389/fphys.2021.618307

Abstract

Prefrontal cortex (PFC) are broadly linked to various aspects of behavior. During sensory discrimination, PFC neurons can encode a range of task related information, including the identity of sensory stimuli and related behavioral outcome. However, it remains largely unclear how different neuron subtypes and local field potential (LFP) oscillation features in the mouse PFC are modulated during sensory discrimination. To understand how excitatory and inhibitory PFC neurons are selectively engaged during sensory discrimination and how their activity relates to LFP oscillations, we used tetrode recordings to probe well-isolated individual neurons, and LFP oscillations, in mice performing a three-choice auditory discrimination task. We found that a majority of PFC neurons, 78% of the 711 recorded individual neurons, exhibited sensory discrimination related responses that are context and task dependent. Using spike waveforms, we classified these responsive neurons into putative excitatory neurons with broad waveforms or putative inhibitory neurons with narrow waveforms, and found that both neuron subtypes were transiently modulated, with individual neurons’ responses peaking throughout the entire duration of the trial. While the number of responsive excitatory neurons remain largely constant throughout the trial, an increasing fraction of inhibitory neurons were gradually recruited as the trial progressed. Further examination of the coherence between individual neurons and LFPs revealed that inhibitory neurons exhibit higher spike-field coherence with LFP oscillations than excitatory neurons during all aspects of the trial and across multiple frequency bands. Together, our results demonstrate that PFC excitatory neurons are continuously engaged during sensory discrimination, whereas PFC inhibitory neurons are increasingly recruited as the trial progresses and preferentially coordinated with LFP oscillations. These results demonstrate increasing involvement of inhibitory neurons in shaping the overall PFC dynamics toward the completion of the sensory discrimination task.

Highlights

The prefrontal cortex (PFC) is known to be critically involved in decision making, and damage to the Prefrontal cortex (PFC) leads to various cognitive deficits (Miller, 2000; Miller and Cohen, 2001; Dalley et al, 2004; Rossi et al, 2007; Gregoriou et al, 2014; Duan et al, 2015; Hanks and Summerfield, 2017; Gritton et al, 2020)
Understanding the different dynamics of excitatory vs. inhibitory neuronal populations in PFC is of great interest in studying PFC involvement in cognitive functions
We distinguished putative excitatory neurons and putative inhibitory neurons based on spike waveforms, and found that inhibitory neurons on average showed peak activity later in the trial compared to excitatory cells

Summary

Introduction

The prefrontal cortex (PFC) is known to be critically involved in decision making, and damage to the PFC leads to various cognitive deficits (Miller, 2000; Miller and Cohen, 2001; Dalley et al, 2004; Rossi et al, 2007; Gregoriou et al, 2014; Duan et al, 2015; Hanks and Summerfield, 2017; Gritton et al, 2020). Calcium imaging of PFC neurons in a go/no-go task further revealed that excitatory neurons exhibit heterogeneous responses, while inhibitory neurons tend to be more correlated within their subtypes (Pinto and Dan, 2015; Kamigaki and Dan, 2017), presumably due to gap junction coupling (Gibson et al, 1999). Parvalbumin-expressing (PV) neurons were shown to respond to various aspect of a task (Pinto and Dan, 2015; Lagler et al, 2016), especially to reward (Kvitsiani et al, 2013; Sparta et al, 2014), whereas somatostatin-expressing (SST) neurons tend to be more selective and respond primarily to sensory stimuli and motor activity (Kvitsiani et al, 2013; Pinto and Dan, 2015)

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Results

Conclusion