Layer 6 ensembles can selectively regulate the behavioral impact and layer-specific representation of sensory deviants.

Jakob Voigts,Christopher A Deister,Christopher I Moore

doi:10.7554/elife.48957

Jakob Voigts, Christopher A Deister + Show 1 more

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https://doi.org/10.7554/elife.48957

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Abstract

Predictive models can enhance the salience of unanticipated input. Here, we tested a key potential node in neocortical model formation in this process, layer (L) 6, using behavioral, electrophysiological and imaging methods in mouse primary somatosensory neocortex. We found that deviant stimuli enhanced tactile detection and were encoded in L2/3 neural tuning. To test the contribution of L6, we applied weak optogenetic drive that changed which L6 neurons were sensory responsive, without affecting overall firing rates in L6 or L2/3. This stimulation selectively suppressed behavioral sensitivity to deviant stimuli, without impacting baseline performance. This stimulation also eliminated deviance encoding in L2/3 but did not impair basic stimulus responses across layers. In contrast, stronger L6 drive inhibited firing and suppressed overall sensory function. These findings indicate that, despite their sparse activity, specific ensembles of stimulus-driven L6 neurons are required to form neocortical predictions, and to realize their behavioral benefit.

Highlights

The six-layered architecture of mammalian neocortex emerged relatively late in evolution
We tested the impact of manipulating Layer 6 (L6) CT cells in a naturalistic and untrained, but well studied and characterized sensory decision-making task, Gap Crossing (Hutson and Masterton, 1986; Figure 1a)
Weak optogenetic drive changed the sensory-responsive L6 ensemble, by facilitating and suppressing different subsets of cells without changing the overall firing rates and reduced their information content about the stimulus. This manipulation removed the encoding of stimulus deviants in layers 2/3 (L2/3)

Summary

Introduction

The six-layered architecture of mammalian neocortex emerged relatively late in evolution. When identical sensory stimuli are repeated and a ‘deviant’ occurs, neocortical neurons often fire differently than they would to the deviant in isolation, or after its repetition (Chater et al, 2006; Rao and Ballard, 1999). Signatures of this computation are found in visual (Courchesne et al, 1975), auditory (Tiitinen et al, 1994; Ulanovsky et al, 2003), and languageprocessing (Kutas and Hillyard, 1980) areas. Stimulus-tuned neurons along the afferent pathway, including at thalamocortical synapses, adapt to repeated stimulation (Chung et al, 2002; Katz et al, 2006; Khatri and Simons, 2007) and subsequent deviant stimuli activate new pools of less adapted neurons, leading to increased neocortical drive

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