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Motor, somatosensory, and executive cortical areas elicit monosynaptic and polysynaptic neuronal activity in the auditory midbrain

Lookup NU author(s): Dr Sasha Gartside, Dr Bas OlthofORCiD, Professor Adrian ReesORCiD

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

© 2024. We recently reported that the central nucleus of the inferior colliculus (the auditory midbrain) is innervated by glutamatergic pyramidal cells originating not only in auditory cortex (AC), but also in multiple ‘non-auditory’ regions of the cerebral cortex. Here, in anaesthetised rats, we used optogenetics and electrical stimulation, combined with recording in the inferior colliculus to determine the functional influence of these descending connections. Specifically, we determined the extent of monosynaptic excitation and the influence of these descending connections on spontaneous activity in the inferior colliculus. A retrograde virus encoding both green fluorescent protein (GFP) and channelrhodopsin (ChR2) injected into the central nucleus of the inferior colliculus (ICC) resulted in GFP expression in discrete groups of cells in multiple areas of the cerebral cortex. Light stimulation of AC and primary motor cortex (M1) caused local activation of cortical neurones and increased the firing rate of neurones in ICC indicating a direct excitatory input from AC and M1 to ICC with a restricted distribution. In naïve animals, electrical stimulation at multiple different sites within M1, secondary motor, somatosensory, and prefrontal cortices increased firing rate in ICC. However, it was notable that stimulation at some adjacent sites failed to influence firing at the recording site in ICC. Responses in ICC comprised singular spikes of constant shape and size which occurred with a short, and fixed latency (∼ 5 ms) consistent with monosynaptic excitation of individual ICC units. Increasing the stimulus current decreased the latency of these spikes, suggesting more rapid depolarization of cortical neurones, and increased the number of (usually adjacent) channels on which a monosynaptic spike was seen, suggesting recruitment of increasing numbers of cortical neurons. Electrical stimulation of cortical regions also evoked longer latency, longer duration increases in firing activity, comprising multiple units with spikes occurring with significant temporal jitter, consistent with polysynaptic excitation. Increasing the stimulus current increased the number of spikes in these polysynaptic responses and increased the number of channels on which the responses were observed, although the magnitude of the responses always diminished away from the most activated channels. Together our findings indicate descending connections from motor, somatosensory and executive cortical regions directly activate small numbers of ICC neurones and that this in turn leads to extensive polysynaptic activation of local circuits within the ICC.


Publication metadata

Author(s): Gartside SE, Olthof BM, Rees A

Publication type: Article

Publication status: Published

Journal: Hearing Research

Year: 2024

Volume: 447

Print publication date: 01/06/2024

Online publication date: 16/04/2024

Acceptance date: 15/04/2024

Date deposited: 08/05/2024

ISSN (print): 0378-5955

ISSN (electronic): 1878-5891

Publisher: Elsevier BV

URL: https://doi.org/10.1016/j.heares.2024.109009

DOI: 10.1016/j.heares.2024.109009

Data Access Statement: Data will be made available on request.


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Funding

Funder referenceFunder name
BB/P003249/1Biotechnology and Biological Sciences Research Council (BBSRC)

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