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Article: Auditory midbrain processing is deferentially modulated by auditory and visual cortices: an auditory fMRI study

TitleAuditory midbrain processing is deferentially modulated by auditory and visual cortices: an auditory fMRI study
Authors
KeywordsAuditory midbrain
Inferior colliculus
Auditory cortex
Visual cortex
fMRI
Rodent
Sound level
Vocalizations
Issue Date2015
PublisherAcademic Press. The Journal's web site is located at http://www.elsevier.com/locate/ynimg
Citation
Neuroimage, 2015, v. 123, p. 22-32 How to Cite?
AbstractThe cortex contains extensive descending projections, yet the impact of cortical input on brainstem processing remains poorly understood. In the central auditory system, the auditory cortex contains direct and indirect pathways (via brainstem cholinergic cells) to nuclei of the auditory midbrain, called the inferior colliculus (IC). While these projections modulate auditory processing throughout the IC, single neuron recordings have samples from only a small fraction of cells during stimulation of the corticofugal pathway. Furthermore, assessments of cortical feedback have not been extended to sensory modalities other than audition. To address these issues, we devised blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) paradigms to measure the sound-evoked responses throughout the rat IC and investigated the effects of bilateral ablation of either auditory or visual cortices. Auditory cortex ablation increased the gain of IC responses to noise stimuli (primarily in the central nucleus of the IC) and decreased response selectivity to forward species-specific vocalizations (versus temporally reversed ones, most prominently in the external cortex of the IC). In contrast, visual cortex ablation decreased the gain and induced a much smaller effect on response selectivity. The results suggest that auditory cortical projections normally exert a large-scale and net suppressive influence on specific IC subnuclei, while visual cortical projections provide a facilitatory influence. Meanwhile, auditory cortical projections enhance the midbrain response selectivity to species-specific vocalizations. We also probed the role of the indirect cholinergic projections in the auditory system in the descending modulation process by pharmacologically blocking muscarinic cholinergic receptors. This manipulation did not affect the gain of IC responses but significantly reduced the response selectivity to vocalizations. The results imply that auditory cortical gain modulation is mediated primarily through direct projections and they point to future investigations of the differential roles of the direct and indirect projections in corticofugal modulation. In summary, our imaging findings demonstrate the large-scale descending influences, from both the auditory and visual cortices, on sound processing in different IC subdivisions. They can guide future studies on the coordinated activity across multiple regions of the auditory network, and its dysfunctions.
Persistent Identifierhttp://hdl.handle.net/10722/220145
ISSN
2023 Impact Factor: 4.7
2023 SCImago Journal Rankings: 2.436
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorGao, PP-
dc.contributor.authorZhang, JW-
dc.contributor.authorFan, SJ-
dc.contributor.authorSanes, DH-
dc.contributor.authorWu, EX-
dc.date.accessioned2015-10-16T06:30:29Z-
dc.date.available2015-10-16T06:30:29Z-
dc.date.issued2015-
dc.identifier.citationNeuroimage, 2015, v. 123, p. 22-32-
dc.identifier.issn1053-8119-
dc.identifier.urihttp://hdl.handle.net/10722/220145-
dc.description.abstractThe cortex contains extensive descending projections, yet the impact of cortical input on brainstem processing remains poorly understood. In the central auditory system, the auditory cortex contains direct and indirect pathways (via brainstem cholinergic cells) to nuclei of the auditory midbrain, called the inferior colliculus (IC). While these projections modulate auditory processing throughout the IC, single neuron recordings have samples from only a small fraction of cells during stimulation of the corticofugal pathway. Furthermore, assessments of cortical feedback have not been extended to sensory modalities other than audition. To address these issues, we devised blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (fMRI) paradigms to measure the sound-evoked responses throughout the rat IC and investigated the effects of bilateral ablation of either auditory or visual cortices. Auditory cortex ablation increased the gain of IC responses to noise stimuli (primarily in the central nucleus of the IC) and decreased response selectivity to forward species-specific vocalizations (versus temporally reversed ones, most prominently in the external cortex of the IC). In contrast, visual cortex ablation decreased the gain and induced a much smaller effect on response selectivity. The results suggest that auditory cortical projections normally exert a large-scale and net suppressive influence on specific IC subnuclei, while visual cortical projections provide a facilitatory influence. Meanwhile, auditory cortical projections enhance the midbrain response selectivity to species-specific vocalizations. We also probed the role of the indirect cholinergic projections in the auditory system in the descending modulation process by pharmacologically blocking muscarinic cholinergic receptors. This manipulation did not affect the gain of IC responses but significantly reduced the response selectivity to vocalizations. The results imply that auditory cortical gain modulation is mediated primarily through direct projections and they point to future investigations of the differential roles of the direct and indirect projections in corticofugal modulation. In summary, our imaging findings demonstrate the large-scale descending influences, from both the auditory and visual cortices, on sound processing in different IC subdivisions. They can guide future studies on the coordinated activity across multiple regions of the auditory network, and its dysfunctions.-
dc.languageeng-
dc.publisherAcademic Press. The Journal's web site is located at http://www.elsevier.com/locate/ynimg-
dc.relation.ispartofNeuroimage-
dc.subjectAuditory midbrain-
dc.subjectInferior colliculus-
dc.subjectAuditory cortex-
dc.subjectVisual cortex-
dc.subjectfMRI-
dc.subjectRodent-
dc.subjectSound level-
dc.subjectVocalizations-
dc.titleAuditory midbrain processing is deferentially modulated by auditory and visual cortices: an auditory fMRI study-
dc.typeArticle-
dc.identifier.emailWu, EX: ewu@eee.hku.hk-
dc.identifier.authorityWu, EX=rp00193-
dc.identifier.doi10.1016/j.neuroimage.2015.08.040-
dc.identifier.pmid26306991-
dc.identifier.scopuseid_2-s2.0-84941649596-
dc.identifier.hkuros255255-
dc.identifier.hkuros268246-
dc.identifier.volume123-
dc.identifier.spage22-
dc.identifier.epage32-
dc.identifier.isiWOS:000363763900003-
dc.publisher.placeUnited States-
dc.identifier.issnl1053-8119-

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