Presynaptic neuronal nicotinic receptors differentially shape select inputs to auditory thalamus and are negatively impacted by aging

Sarah Y. Sottile, Troy A. Hackett, Rui Cai, Lynne Ling, Daniel A. Llano, Donald M. Caspary

Research output: Contribution to journalArticlepeer-review

Abstract

Acetylcholine (ACh) is a potent neuromodulator capable of modifying patterns of acoustic information flow. In auditory cortex, cholinergic systems have been shown to increase salience/gain while suppressing extraneous information. However, the mechanism by which cholinergic circuits shape signal processing in the auditory thalamus (medial geniculate body, MGB) is poorly understood. The present study, in male Fischer Brown Norway rats, seeks to determine the location and function of presynaptic neuronal nicotinic ACh receptors (nAChRs) at the major inputs to MGB and characterize how nAChRs change during aging. In vitro electrophysiological/optogenetic methods were used to examine responses of MGB neurons after activation of nAChRs during a paired-pulse paradigm. Presynaptic nAChR activation increased responses evoked by stimulation of excitatory corticothalamic and inhibitory tectothalamic terminals. Conversely,nAChRactivation appeared to have little effect on evoked responses from inhibitory thalamic reticular nucleus and excitatory tectothalamic terminals. In situ hybridization data showed nAChR subunit transcripts in GABAergic inferior colliculus neurons and glutamatergic auditory cortical neurons supporting the present slice findings. Responses to nAChR activation at excitatory corticothalamic and inhibitory tectothalamic inputs were diminished by aging. These findings suggest that cholinergic input to the MGB increases the strength of tectothalamic inhibitory projections, potentially improving the signal-to-noise ratio and signal detection while increasing corticothalamic gain, which may facilitate top-down identification of stimulus identity. These mechanisms appear to be affected negatively by aging, potentially diminishing speech perception in noisy environments. Cholinergic inputs to the MGB appear to maximize sensory processing by adjusting both top-down and bottom-up mechanisms in conditions of attention and arousal.

Original languageEnglish (US)
Pages (from-to)11377-11389
Number of pages13
JournalJournal of Neuroscience
Volume37
Issue number47
DOIs
StatePublished - Nov 22 2017

Keywords

  • Aging
  • Attention
  • Auditory
  • Nicotinic
  • Sensory processing
  • Thalamus

ASJC Scopus subject areas

  • Neuroscience(all)

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