Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets

<p>Cortical acetylcholine (ACh) release has been linked to various cognitive functions, including perceptual learning. We have previously shown that cortical cholinergic innervation is necessary for accurate sound localization in ferrets, as well as for their ability to adapt with training to...

Full description

Bibliographic Details
Main Authors: Nodal, FR, Leach, ND, Keating, P, Dahmen, JC, Zhao, D, King, AJ, Bajo, VM
Format: Journal article
Language:English
Published: Elsevier 2024
_version_ 1811139535153659904
author Nodal, FR
Leach, ND
Keating, P
Dahmen, JC
Zhao, D
King, AJ
Bajo, VM
author_facet Nodal, FR
Leach, ND
Keating, P
Dahmen, JC
Zhao, D
King, AJ
Bajo, VM
author_sort Nodal, FR
collection OXFORD
description <p>Cortical acetylcholine (ACh) release has been linked to various cognitive functions, including perceptual learning. We have previously shown that cortical cholinergic innervation is necessary for accurate sound localization in ferrets, as well as for their ability to adapt with training to altered spatial cues. To explore whether these behavioral deficits are associated with changes in the response properties of cortical neurons, we recorded neural activity in the primary auditory cortex (A1) of anesthetized ferrets in which cholinergic inputs had been reduced by making bilateral injections of the immunotoxin ME20.4-SAP in the nucleus basalis (NB) prior to training the animals. The pattern of spontaneous activity of A1 units recorded in the ferrets with cholinergic lesions (NB ACh<sup>&ndash;</sup>) was similar to that in controls, although the proportion of burst-type units was significantly lower. Depletion of ACh also resulted in more synchronous activity in A1. No changes in thresholds, frequency tuning or in the distribution of characteristic frequencies were found in these animals. When tested with normal acoustic inputs, the spatial sensitivity of A1 neurons in the NB ACh<sup>&ndash;</sup>&nbsp;ferrets and the distribution of their preferred interaural level differences also closely resembled those found in control animals, indicating that these properties had not been altered by sound localization training with one ear occluded. Simulating the animals&rsquo; previous experience with a virtual earplug in one ear reduced the contralateral preference of A1 units in both groups, but caused azimuth sensitivity to change in slightly different ways, which may reflect the modest adaptation observed in the NB ACh<sup>&ndash;</sup>&nbsp;group. These results show that while ACh is required for behavioral adaptation to altered spatial cues, it is not required for maintenance of the spectral and spatial response properties of A1 neurons.</p>
first_indexed 2024-09-25T04:07:38Z
format Journal article
id oxford-uuid:b3fad66e-e09f-43a1-80bd-fc96237f4826
institution University of Oxford
language English
last_indexed 2024-09-25T04:07:38Z
publishDate 2024
publisher Elsevier
record_format dspace
spelling oxford-uuid:b3fad66e-e09f-43a1-80bd-fc96237f48262024-05-31T08:39:30ZNeural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferretsJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:b3fad66e-e09f-43a1-80bd-fc96237f4826EnglishSymplectic ElementsElsevier2024Nodal, FRLeach, NDKeating, PDahmen, JCZhao, DKing, AJBajo, VM<p>Cortical acetylcholine (ACh) release has been linked to various cognitive functions, including perceptual learning. We have previously shown that cortical cholinergic innervation is necessary for accurate sound localization in ferrets, as well as for their ability to adapt with training to altered spatial cues. To explore whether these behavioral deficits are associated with changes in the response properties of cortical neurons, we recorded neural activity in the primary auditory cortex (A1) of anesthetized ferrets in which cholinergic inputs had been reduced by making bilateral injections of the immunotoxin ME20.4-SAP in the nucleus basalis (NB) prior to training the animals. The pattern of spontaneous activity of A1 units recorded in the ferrets with cholinergic lesions (NB ACh<sup>&ndash;</sup>) was similar to that in controls, although the proportion of burst-type units was significantly lower. Depletion of ACh also resulted in more synchronous activity in A1. No changes in thresholds, frequency tuning or in the distribution of characteristic frequencies were found in these animals. When tested with normal acoustic inputs, the spatial sensitivity of A1 neurons in the NB ACh<sup>&ndash;</sup>&nbsp;ferrets and the distribution of their preferred interaural level differences also closely resembled those found in control animals, indicating that these properties had not been altered by sound localization training with one ear occluded. Simulating the animals&rsquo; previous experience with a virtual earplug in one ear reduced the contralateral preference of A1 units in both groups, but caused azimuth sensitivity to change in slightly different ways, which may reflect the modest adaptation observed in the NB ACh<sup>&ndash;</sup>&nbsp;group. These results show that while ACh is required for behavioral adaptation to altered spatial cues, it is not required for maintenance of the spectral and spatial response properties of A1 neurons.</p>
spellingShingle Nodal, FR
Leach, ND
Keating, P
Dahmen, JC
Zhao, D
King, AJ
Bajo, VM
Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title_full Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title_fullStr Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title_full_unstemmed Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title_short Neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
title_sort neural processing in the primary auditory cortex following cholinergic lesions of the basal forebrain in ferrets
work_keys_str_mv AT nodalfr neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT leachnd neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT keatingp neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT dahmenjc neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT zhaod neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT kingaj neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets
AT bajovm neuralprocessingintheprimaryauditorycortexfollowingcholinergiclesionsofthebasalforebraininferrets