Broadband Entrainment of Striatal Low-Threshold Spike Interneurons.

Juan C Morales,Charles J Wilson,Soomin C Song,Matthew H Higgs

doi:10.3389/fncir.2020.00036

Abstract

Striatal interneurons and spiny projection (SP) neurons are differentially tuned to spectral components of their input. Previous studies showed that spike responses of somatostatin/NPY-expressing low threshold spike (LTS) interneurons have broad frequency tuning, setting these cells apart from other striatal GABAergic interneurons and SP neurons. We investigated the mechanism of LTS interneuron spiking resonance and its relationship to non-spiking membrane impedance resonance, finding that abolition of impedance resonance did not alter spiking resonance. Because LTS interneurons are pacemakers whose rhythmic firing is perturbed by synaptic input, we tested the hypothesis that their spiking resonance arises from their phase resetting properties. Phase resetting curves (PRCs) were measured in LTS interneurons and SP neurons and used to make phase-oscillator models of both cell types. The models reproduced the broad tuning of LTS interneurons, and the differences from SP neurons. The spectral components of the PRC predicted each cell’s sensitivity to corresponding input frequencies. LTS interneuron PRCs contain larger high-frequency components than SP neuron PRCs, providing enhanced responses to input frequencies above the cells’ average firing rates. Thus, LTS cells can be entrained by input oscillations to which SP neurons are less responsive. These findings suggest that feedforward inhibition by LTS interneurons may regulate SP neurons’ entrainment by oscillatory afferents.

Highlights

Oscillatory synaptic inputs can entrain spiking in neurons, but in each cell type some input frequencies are more effective than others
In the work reported here we show that membrane impedance resonance has no measurable contribution to the spiking resonance of striatal lowthreshold spiking (LTS) interneurons or their entrainment by periodic current waveforms
Striatal LTS interneurons were identified by fluorescence microscopy in brain slices from NPY-green fluorescent protein (GFP) mice at the time of recording

Summary

Introduction

Oscillatory synaptic inputs can entrain spiking in neurons, but in each cell type some input frequencies are more effective than others. Frequency-selectivity is one way in which cell types within a local circuit can specialize in the processing of complex input patterns This phenomenon, called spiking resonance, applies to oscillatory signals that are large and distinguished from other components of the input, and to the multiple frequency components embedded in a broadband synaptic input (e.g., Wilson et al, 2018). Some have a relatively fixed frequency sensitivity and in others the frequency sensitivity can be altered flexibly (Beatty et al, 2015) These differences are frequency signatures of cell types and determine the rate and timing of their responses to Striatal LTS Cells specific patterns of synaptic input. LTS interneurons provide feedforward inhibition to SP neurons, and their broad frequency sensitivity might oppose SP cell entrainment over a range of input frequencies, altering their effective frequency tuning

Methods

Results

Conclusion