scholarly journals Dopamine in the songbird auditory cortex shapes auditory preference

2019 ◽  
Author(s):  
Helena J. Barr ◽  
Erin M. Wall ◽  
Sarah C. Woolley

ABSTRACTIn vocal communication, vocal signals can provide listeners with information and also elicit motivated responses. Auditory cortical and mesolimbic reward circuits are often considered to have distinct roles in these processes, with auditory cortical circuits responsible for detecting and discriminating sounds and mesolimbic circuits ascribing salience and modulating preference for those sounds. Here, we investigated whether dopamine within auditory cortical circuits themselves can shape the incentive salience of a vocal signal. Using female zebra finches, who show natural preferences for vocal signals produced by males (‘songs’), we found that pairing passive song playback with pharmacological manipulations of dopamine in the secondary auditory cortex drives changes to song preferences. Plasticity of song preferences by dopamine lasted for at least one week and was not influenced by norepinephrine manipulations. These data suggest that dopamine acting directly in sensory processing areas can shape the incentive salience of communication signals.

Author(s):  
Peter Gombkoto ◽  
Matthew Gielow ◽  
Peter Varsanyi ◽  
Candice Chavez ◽  
Laszlo Zaborszky

AbstractBasal forebrain (BF) cholinergic neurons provide the cerebral cortex with acetylcholine. Despite the long-established involvement of these cells in sensory processing, attention, and memory, the mechanisms by which cholinergic signaling regulates cognitive processes remain elusive. In this study, we recorded spiking and local field potential data simultaneously from several locations in the BF, and sites in the orbitofrontal and visual cortex in transgenic ChAT-Cre rats performing a visual discrimination task. We observed distinct differences in the fine spatial distributions of gamma coherence values between specific basalo-cortical and cortico-cortical sites that shifted across task phases. Additionally, cholinergic firing induced spatial changes in cortical gamma power, and optogenetic activation of BF increased coherence between specific cortico-cortical sites, suggesting that the cholinergic system contributes to selective modulation of cortico-cortical circuits. Furthermore, the results suggest that cells in specific BF locations are dynamically recruited across behavioral epochs to coordinate interregional cortical processes underlying cognition.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Adam R. Fishbein ◽  
Nora H. Prior ◽  
Jane A. Brown ◽  
Gregory F. Ball ◽  
Robert J. Dooling

AbstractStudies of acoustic communication often focus on the categories and units of vocalizations, but subtle variation also occurs in how these signals are uttered. In human speech, it is not only phonemes and words that carry information but also the timbre, intonation, and stress of how speech sounds are delivered (often referred to as “paralinguistic content”). In non-human animals, variation across utterances of vocal signals also carries behaviorally relevant information across taxa. However, the discriminability of these cues has been rarely tested in a psychophysical paradigm. Here, we focus on acoustic communication in the zebra finch (Taeniopygia guttata), a songbird species in which the male produces a single stereotyped motif repeatedly in song bouts. These motif renditions, like the song repetitions of many birds, sound very similar to the casual human listener. In this study, we show that zebra finches can easily discriminate between the renditions, even at the level of single song syllables, much as humans can discriminate renditions of speech sounds. These results support the notion that sensitivity to fine acoustic details may be a primary channel of information in zebra finch song, as well as a shared, foundational property of vocal communication systems across species.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jennifer Resnik ◽  
Daniel B Polley

Cortical neurons remap their receptive fields and rescale sensitivity to spared peripheral inputs following sensory nerve damage. To address how these plasticity processes are coordinated over the course of functional recovery, we tracked receptive field reorganization, spontaneous activity, and response gain from individual principal neurons in the adult mouse auditory cortex over a 50-day period surrounding either moderate or massive auditory nerve damage. We related the day-by-day recovery of sound processing to dynamic changes in the strength of intracortical inhibition from parvalbumin-expressing (PV) inhibitory neurons. Whereas the status of brainstem-evoked potentials did not predict the recovery of sensory responses to surviving nerve fibers, homeostatic adjustments in PV-mediated inhibition during the first days following injury could predict the eventual recovery of cortical sound processing weeks later. These findings underscore the potential importance of self-regulated inhibitory dynamics for the restoration of sensory processing in excitatory neurons following peripheral nerve injuries.


2021 ◽  
Author(s):  
Nasim Winchester Vahidi

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.


2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Jonathan I. Benichov ◽  
Daniela Vallentin

AbstractVocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.


2020 ◽  
Vol 30 (7) ◽  
pp. 3895-3909
Author(s):  
Stylianos Kouvaros ◽  
Manoj Kumar ◽  
Thanos Tzounopoulos

Abstract Cortical inhibition is essential for brain activity and behavior. Yet, the mechanisms that modulate cortical inhibition and their impact on sensory processing remain less understood. Synaptically released zinc, a neuromodulator released by cortical glutamatergic synaptic vesicles, has emerged as a powerful modulator of sensory processing and behavior. Despite the puzzling finding that the vesicular zinc transporter (ZnT3) mRNA is expressed in cortical inhibitory interneurons, the actions of synaptic zinc in cortical inhibitory neurotransmission remain unknown. Using in vitro electrophysiology and optogenetics in mouse brain slices containing the layer 2/3 (L2/3) of auditory cortex, we discovered that synaptic zinc increases the quantal size of inhibitory GABAergic neurotransmission mediated by somatostatin (SOM)- but not parvalbumin (PV)-expressing neurons. Using two-photon imaging in awake mice, we showed that synaptic zinc is required for the effects of SOM- but not PV-mediated inhibition on frequency tuning of principal neurons. Thus, cell-specific zinc modulation of cortical inhibition regulates frequency tuning.


2019 ◽  
Vol 94 (Suppl. 1-4) ◽  
pp. 51-60
Author(s):  
Julie E. Elie ◽  
Susanne Hoffmann ◽  
Jeffery L. Dunning ◽  
Melissa J. Coleman ◽  
Eric S. Fortune ◽  
...  

Acoustic communication signals are typically generated to influence the behavior of conspecific receivers. In songbirds, for instance, such cues are routinely used by males to influence the behavior of females and rival males. There is remarkable diversity in vocalizations across songbird species, and the mechanisms of vocal production have been studied extensively, yet there has been comparatively little emphasis on how the receiver perceives those signals and uses that information to direct subsequent actions. Here, we emphasize the receiver as an active participant in the communication process. The roles of sender and receiver can alternate between individuals, resulting in an emergent feedback loop that governs the behavior of both. We describe three lines of research that are beginning to reveal the neural mechanisms that underlie the reciprocal exchange of information in communication. These lines of research focus on the perception of the repertoire of songbird vocalizations, evaluation of vocalizations in mate choice, and the coordination of duet singing.


2003 ◽  
Vol 89 (4) ◽  
pp. 2194-2207 ◽  
Author(s):  
Steven J. Eliades ◽  
Xiaoqin Wang

Little is known about sensory-motor interaction in the auditory cortex of primates at the level of single neurons and its role in supporting vocal communication. The present study investigated single-unit activities in the auditory cortex of a vocal primate, the common marmoset ( Callithrix jacchus), during self-initiated vocalizations. We found that 1) self-initiated vocalizations resulted in suppression of neural discharges in a majority of auditory cortical neurons. The vocalization-induced inhibition suppressed both spontaneous and stimulus-driven discharges. Suppressed units responded poorly to external acoustic stimuli during vocalization. 2) Vocalization-induced suppression began several hundred milliseconds prior to the onset of vocalization. 3) The suppression of cortical discharges reduced neural firings to below the rates expected from a unit's rate-level function, adjusted for known subcortical attenuation, and therefore was likely not entirely caused by subcortical attenuation mechanisms. 4) A smaller population of auditory cortical neurons showed increased discharges during self-initiated vocalizations. This vocalization-related excitation began after the onset of vocalization and is likely the result of acoustic feedback. Units showing this excitation responded nearly normally to external stimuli during vocalization. Based on these findings, we propose that the suppression of auditory cortical neurons, possibly originating from cortical vocal production centers, acts to increase the dynamic range of cortical responses to vocalization feedback for self monitoring. The excitatory responses, on the other hand, likely play a role in maintaining hearing sensitivity to the external acoustic environment during vocalization.


2015 ◽  
Vol 76 (1) ◽  
pp. 47-63 ◽  
Author(s):  
Laura E. Matheson ◽  
Herie Sun ◽  
Jon T. Sakata

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