Anatomical and Functional Organization of Inhibitory Circuits in the Songbird Auditory Forebrain

Recent studies on the anatomical and functional organization of GABAergic networks in central auditory circuits of the zebra finch have highlighted the strong impact of inhibitory mechanisms on both the central encoding and processing of acoustic information in a vocal learning species. Most of this work has focused on the caudomedial nidopallium (NCM), a forebrain area postulated to be the songbird analogue of the mammalian auditory association cortex. NCM houses neurons with selective responses to conspecific songs and is a site thought to house auditory memories required for vocal learning and, likely, individual identification. Here we review our recent work on the anatomical distribution of GABAergic cells in NCM, their engagement in response to song and the roles for inhibitory transmission in the physiology of NCM at rest and during the processing of natural communication signals. GABAergic cells are highly abundant in the songbird auditory forebrain and account for nearly half of the overall neuronal population in NCM with a large fraction of these neurons activated by song in freely-behaving animals. GABAergic synapses provide considerable local, tonic inhibition to NCM neurons at rest and, during sound processing, may contain the spread of excitation away from un-activated or quiescent parts of the network. Finally, we review our work showing that GABAA-mediated inhibition directly regulates the temporal organization of song-driven responses in awake songbirds, and appears to enhance the reliability of auditory encoding in NCM.

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Spatial and Temporal Organization of Composite Receptive Fields in the Songbird Auditory Forebrain

10.1101/2021.07.21.453115 ◽

2021 ◽

Author(s):

Nasim Winchester Vahidi

Keyword(s):

Vocal Communication ◽

Receptive Fields ◽

Temporal Organization ◽

Quadratic Model ◽

Bird Songs ◽

Communication Signals ◽

Complete Representation ◽

Auditory Forebrain ◽

Neuron Populations ◽

Classical Models

The mechanisms underlying how single auditory neurons and neuron populations encode natural and acoustically complex vocal signals, such as human speech or bird songs, are not well understood. Classical models focus on individual neurons, whose spike rates vary systematically as a function of change in a small number of simple acoustic dimensions. However, neurons in the caudal medial nidopallium (NCM), an auditory forebrain region in songbirds that is analogous to the secondary auditory cortex in mammals, have composite receptive fields (CRFs) that comprise multiple acoustic features tied to both increases and decreases in firing rates. Here, we investigated the anatomical organization and temporal activation patterns of auditory CRFs in European starlings exposed to natural vocal communication signals (songs). We recorded extracellular electrophysiological responses to various bird songs at auditory NCM sites, including both single and multiple neurons, and we then applied a quadratic model to extract large sets of CRF features that were tied to excitatory and suppressive responses at each measurement site. We found that the superset of CRF features yielded spatially and temporally distributed, generalizable representations of a conspecific song. Individual sites responded to acoustically diverse features, as there was no discernable organization of features across anatomically ordered sites. The CRF features at each site yielded broad, temporally distributed responses that spanned the entire duration of many starling songs, which can last for 50 s or more. Based on these results, we estimated that a nearly complete representation of any conspecific song, regardless of length, can be obtained by evaluating populations as small as 100 neurons. We conclude that natural acoustic communication signals drive a distributed yet highly redundant representation across the songbird auditory forebrain, in which adjacent neurons contribute to the encoding of multiple diverse and time-varying spectro-temporal features.

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Auditory-Somatosensory Multisensory Processing in Auditory Association Cortex: An fMRI Study

Journal of Neurophysiology ◽

10.1152/jn.2002.88.1.540 ◽

2002 ◽

Vol 88 (1) ◽

pp. 540-543 ◽

Cited By ~ 244

Author(s):

John J. Foxe ◽

Glenn R. Wylie ◽

Antigona Martinez ◽

Charles E. Schroeder ◽

Daniel C. Javitt ◽

...

Keyword(s):

Auditory Cortex ◽

Multisensory Integration ◽

Multisensory Processing ◽

Primary Auditory Cortex ◽

Superior Temporal Gyrus ◽

Brain Regions ◽

Association Cortex ◽

Convergence Region ◽

Auditory Cortices ◽

Auditory Association Cortex

Using high-field (3 Tesla) functional magnetic resonance imaging (fMRI), we demonstrate that auditory and somatosensory inputs converge in a subregion of human auditory cortex along the superior temporal gyrus. Further, simultaneous stimulation in both sensory modalities resulted in activity exceeding that predicted by summing the responses to the unisensory inputs, thereby showing multisensory integration in this convergence region. Recently, intracranial recordings in macaque monkeys have shown similar auditory-somatosensory convergence in a subregion of auditory cortex directly caudomedial to primary auditory cortex (area CM). The multisensory region identified in the present investigation may be the human homologue of CM. Our finding of auditory-somatosensory convergence in early auditory cortices contributes to mounting evidence for multisensory integration early in the cortical processing hierarchy, in brain regions that were previously assumed to be unisensory.

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Tonotopic organization of human auditory association cortex

Brain Research ◽

10.1016/0006-8993(94)90460-x ◽

1994 ◽

Vol 663 (1) ◽

pp. 38-50 ◽

Cited By ~ 28

Author(s):

Selene Cansino ◽

Samuel J. Williamson ◽

Daniel Karron

Keyword(s):

Association Cortex ◽

Tonotopic Organization ◽

Auditory Association Cortex

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Response plasticity of single neurons in rabbit auditory association cortex during tone-signalled learning

Brain Research ◽

10.1016/0006-8993(82)91168-4 ◽

1982 ◽

Vol 246 (2) ◽

pp. 205-215 ◽

Cited By ~ 50

Author(s):

Nina Kraus ◽

John F. Disterhoft

Keyword(s):

Association Cortex ◽

Single Neurons ◽

Auditory Association Cortex

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Reduced Pyramidal Cell Somal Volume in Auditory Association Cortex of Subjects with Schizophrenia

Neuropsychopharmacology ◽

10.1038/sj.npp.1300120 ◽

2002 ◽

Vol 28 (3) ◽

pp. 599-609 ◽

Cited By ~ 68

Author(s):

Robert A Sweet ◽

Joseph N Pierri ◽

Sungyoung Auh ◽

Allan R Sampson ◽

David A Lewis

Keyword(s):

Pyramidal Cell ◽

Association Cortex ◽

Auditory Association Cortex

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Toward a Synthesis of Cellular Auditory Forebrain Functional Organization

The Auditory Cortex ◽

10.1007/978-1-4419-0074-6_32 ◽

2010 ◽

pp. 679-686

Author(s):

Jeffery A. Winer ◽

Christoph E. Schreiner

Keyword(s):

Functional Organization ◽

Auditory Forebrain

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Contribution of Human Prefrontal Cortex to Delay Performance

Journal of Cognitive Neuroscience ◽

10.1162/089892998562636 ◽

1998 ◽

Vol 10 (2) ◽

pp. 167-177 ◽

Cited By ~ 149

Author(s):

Linda L. Chao ◽

Robert T. Knight

Keyword(s):

Prefrontal Cortex ◽

Neural Activity ◽

Dorsolateral Prefrontal Cortex ◽

Silent Period ◽

Primary Auditory Cortex ◽

Association Cortex ◽

Focal Lesions ◽

Delay Performance ◽

Dorsolateral Prefrontal ◽

Auditory Association Cortex

Neurological patients with focal lesions in the dorsolateral prefrontal cortex and age-matched control subjects were tested on an auditory version of the delayed-match-to-sample task employing environmental sounds. Subjects had to indicate whether a cue (S1) and a subsequent target sound (S2) were identical. On some trials, S1 and S2 were separated by a silent period of 5 sec. On other trials, the 5-sec delay between S1 and S2 was filled with irrelevant tone pips that served as distractors. Behaviorally, frontal patients were impaired by the presence of distractors. Electrophysiologically, patients generated enhanced primary auditory cortex-evoked responses to the tone pips, supporting a failure in inhibitory control of sensory processing after prefrontal damage. Intrahemispheric reductions of neural activity generated in the auditory association cortex and additional intrahemispheric reductions of attention-related frontal activity were also observed in the prefrontal patients. Together, these findings suggest that the dorsolateral prefrontal cortex is crucial for gating distracting information as well as maintaining distributed intrahemispheric neural activity during auditory working memory.

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