Cholinergic Modulation of Stimulus-Specific Adaptation in the Inferior Colliculus.
Neural encoding of an ever-changing acoustic environment is a complex and demanding process that depends on modulation by neuroactive substances. Some neurons of the inferior colliculus (IC) exhibit "stimulus-specific adaptation" (SSA), i.e., a decrease in their response to a repetitive sound, but not to a rare one. Previous studies have demonstrated that acetylcholine (ACh) alters the frequency response areas of auditory neurons and therefore is important in the encoding of spectral information. Here, we address how microiontophoretic application of ACh modulates SSA in the IC of the anesthetized rat. We found that ACh decreased SSA in IC neurons by increasing the response to the repetitive tone. This effect was mainly mediated by muscarinic receptors. The strength of the cholinergic modulation depended on the baseline SSA level, exerting its greatest effect on neurons with intermediate SSA responses across IC subdivisions. Our data demonstrate that the increased availability of ACh exerts transient functional changes in partially adapting IC neurons, enhancing the sensory encoding of the ongoing stimulation. This effect potentially contributes to the propagation of ascending sensory-evoked afferent activity through the thalamus en route to the cortex.


CONCLUSIONS
Neural encoding of an ever-changing acoustic environment is a complex and demanding task that may depend on the available levels of neuroactive substances. We explored how the cholinergic inputs affect the responses of neurons in the auditory midbrain that exhibit different degrees of stimulus-specific adaptation (SSA), i.e., a specific decrease in their response to a repeated sound that does not generalize to other, rare sounds. This work addresses the role of cholinergic synaptic inputs as well as the contribution of the muscarinic and nicotinic receptors on SSA. This is the first report on the role of neuromodulation on SSA, and the results contribute to our understanding of the cellular bases for processing low- and high-probability sounds.
Auditory Neuroscience Laboratory, Institute of Neuroscience of Castilla y León and.
Yaneri A
http://orcid.org/0000-0002-7031-6970
YA
Ayala
Auditory Neuroscience Laboratory, Institute of Neuroscience of Castilla y León and Department of Cell Biology and Pathology, Faculty of Medicine, University of Salamanca, 37007 Salamanca, Spain msm@usal.es.
Manuel S
http://orcid.org/0000-0003-0168-7572
MS
Malmierca
D000109:Acetylcholine / Q000494:pharmacology; D000161:Acoustic Stimulation; D000162:Acoustics; D000200:Action Potentials / Q000187:drug effects*; D000222:Adaptation, Physiological / Q000502:physiology*; D000818:Animals; D016009:Chi-Square Distribution; D018678:Cholinergic Agents / Q000494:pharmacology*; D018680:Cholinergic Antagonists / Q000494:pharmacology; D005260:Female; D007245:Inferior Colliculi / Q000166:cytology*; D007478:Iontophoresis; D008464:Mecamylamine / Q000494:pharmacology; D009474:Neurons / Q000187:drug effects* / Q000502:physiology*; D051381:Rats; D020318:Rats, Long-Evans; D017207:Rats, Sprague-Dawley; D011930:Reaction Time / Q000187:drug effects; D012601:Scopolamine / Q000494:pharmacology
D018678:Cholinergic Agents; D018680:Cholinergic Antagonists; D008464:Mecamylamine; D012601:Scopolamine; D000109:Acetylcholine
SSA; acetylcholine; attention; auditory; microiontophoresis; neuromodulators