High-frequency burst spiking in layer 5 thick-tufted pyramids of rat primary somatosensory cortex encodes exploratory touch

Christiaan P J De Kock,Jean Pie,Jean Pie,Jean Pie,Rebecca A Mease,Jason M Guest,Huibert D Mansvelder,Huibert D Mansvelder,Anton W Pieneman,Arco Bast,Marcel Oberlaender,Anton W Pieneman,Bert Sakmann

doi:10.1038/s42003-021-02241-8

Abstract

Diversity of cell-types that collectively shape the cortical microcircuit ensures the necessary computational richness to orchestrate a wide variety of behaviors. The information content embedded in spiking activity of identified cell-types remain unclear to a large extent. Here, we recorded spike responses upon whisker touch of anatomically identified excitatory cell-types in primary somatosensory cortex in naive, untrained rats. We find major differences across layers and cell-types. The temporal structure of spontaneous spiking contains high-frequency bursts (≥100 Hz) in all morphological cell-types but a significant increase upon whisker touch is restricted to layer L5 thick-tufted pyramids (L5tts) and thus provides a distinct neurophysiological signature. We find that whisker touch can also be decoded from L5tt bursting, but not from other cell-types. We observed high-frequency bursts in L5tts projecting to different subcortical regions, including thalamus, midbrain and brainstem. We conclude that bursts in L5tts allow accurate coding and decoding of exploratory whisker touch.

Highlights

Diversity of cell-types that collectively shape the cortical microcircuit ensures the necessary computational richness to orchestrate a wide variety of behaviors
To study layer- and cell-type-specific representation of untrained, exploratory whisker touches in the primary somatosensory cortex of awake rats, loose-patch recordings were combined with high-speed videography of whisker position
Touch did not increase spiking activity in this L5 slendertufted (L5st) example (Fig. 1g), contrasting the layer 5 (L5) thick-tufted pyramids (L5tts) example, which showed a clear increase in spiking activity upon touch

Summary

Introduction

Diversity of cell-types that collectively shape the cortical microcircuit ensures the necessary computational richness to orchestrate a wide variety of behaviors. The temporal structure of spontaneous spiking contains high-frequency bursts (≥100 Hz) in all morphological cell-types but a significant increase upon whisker touch is restricted to layer L5 thick-tufted pyramids (L5tts) and provides a distinct neurophysiological signature. L(ayer) 5 consists of an intermingled population of two major output neurons: L5 intratelencephalic (IT) and L5 pyramidal tract (PT) neurons, respectively[1], commonly referred to as L5 slendertufted (L5st) and L5 thick-tufted (L5tt) pyramids These two L5 output cell types differ in key structural and functional properties[6,7,8], including afferent input sources[9] and output projection targets[8,10,11]. In auditory and somatosensory cortices, functional properties correlate to L5st versus L5tt identity[8,18,19]

Methods

Results

Conclusion