Developmental divergence of sensory stimulus representation in cortical interneurons

Rahel Kastli,Theofanis Karayannis,Asim Iqbal,Fritjof Helmchen,Rasmus Vighagen,Alexander Van Der Bourg,Daniel Kirschenbaum,Adriano Aguzzi,Fabian F Voigt,Ali Özgür Argunsah

doi:10.1038/s41467-020-19427-z

Rahel Kastli, Theofanis Karayannis + Show 8 more

Open Access

https://doi.org/10.1038/s41467-020-19427-z

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Abstract

Vasocative-intestinal-peptide (VIP+) and somatostatin (SST+) interneurons are involved in modulating barrel cortex activity and perception during active whisking. Here we identify a developmental transition point of structural and functional rearrangements onto these interneurons around the start of active sensation at P14. Using in vivo two-photon Ca2+ imaging, we find that before P14, both interneuron types respond stronger to a multi-whisker stimulus, whereas after P14 their responses diverge, with VIP+ cells losing their multi-whisker preference and SST+ neurons enhancing theirs. Additionally, we find that Ca2+ signaling dynamics increase in precision as the cells and network mature. Rabies virus tracings followed by tissue clearing, as well as photostimulation-coupled electrophysiology reveal that SST+ cells receive higher cross-barrel inputs compared to VIP+ neurons at both time points. In addition, whereas prior to P14 both cell types receive direct input from the sensory thalamus, after P14 VIP+ cells show reduced inputs and SST+ cells largely shift to motor-related thalamic nuclei.

Highlights

Vasocative-intestinal-peptide (VIP+) and somatostatin (SST+) interneurons are involved in modulating barrel cortex activity and perception during active whisking
We observed prominent Ca2+ transients in both IN types that correlated with the activity of the surrounding cells (Figs. 1c and S1a), indicating that they receive input capable of driving action potentials before the onset of active whisking
To test if the same is true for VIP+ and SST+ INs, we compared the correlations of spontaneous activity within each IN population before and after postnatal day 14 (P14) and found a significant drop of co-activation with time (Fig. 1e)

Summary

Introduction

Vasocative-intestinal-peptide (VIP+) and somatostatin (SST+) interneurons are involved in modulating barrel cortex activity and perception during active whisking. We further hypothesized that these INs would be differently engaged by these stimulation paradigms prior to P14, when topdown modulation is absent and discrimination of fine features through the somatosensory system is probably not yet developed When we tested these hypotheses, we found that the strength of activation of VIP+ and SST+ INs depends on the nature of the presented stimulus. We find that compared to the single-whisker deflection, the multi-whisker stimulation leads to a higher activation of both cell types before P14, a phenomenon only maintained in SST+ after the onset of whisking These response alterations are accompanied by a significant rearrangement of thalamic connections onto both VIP+ and SST+ INs in the same time window, later than any other thalamo-cortical connectivity restructuring reported to date

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