Putting it in Context: Linking Auditory Processing with Social Behavior Circuits in the Vertebrate Brain

Petersen, Christopher L.; Hurley, Laura M.

doi:10.1093/icb/icx055

Cited by 20 publications

(14 citation statements)

References 116 publications

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“…SSA first emerges in the auditory system at the level of the inferior colliculus (IC), mainly in its nonlemniscal portion (i.e., the IC cortices) [46]. As a site of convergence of both ascending and descending auditory pathways, the IC plays a key role in processing surprising sounds [47] and shaping the auditory context [48]. The complex computational network of the IC integrates excitatory, inhibitory, and rich neuromodulatory input [49,50], which includes dopaminergic innervation from the thalamic subparafascicular nucleus (SPF) [51][52][53][54][55][56][57][58].…”

Section: Introductionmentioning

confidence: 99%

Dopamine modulates subcortical responses to surprising sounds

et al. 2020

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Dopamine guides behavior and learning through pleasure, according to classic understanding. Dopaminergic neurons are traditionally thought to signal positive or negative prediction errors (PEs) when reward expectations are, respectively, exceeded or not matched. These signed PEs are quite different from the unsigned PEs, which report surprise during sensory processing. But mounting theoretical accounts from the predictive processing framework postulate that dopamine, as a neuromodulator, could potentially regulate the postsynaptic gain of sensory neurons, thereby scaling unsigned PEs according to their expected precision or confidence. Despite ample modeling work, the physiological effects of dopamine on the processing of surprising sensory information are yet to be addressed experimentally. In this study, we tested how dopamine modulates midbrain processing of unexpected tones. We recorded extracellular responses from the rat inferior colliculus to oddball and cascade sequences, before, during, and after the microiontophoretic application of dopamine or eticlopride (a D 2-like receptor antagonist). Results demonstrate that dopamine reduces the net neuronal responsiveness exclusively to unexpected sensory input without significantly altering the processing of expected input. We conclude that dopaminergic projections from the thalamic subparafascicular nucleus to the inferior colliculus could encode the expected precision of unsigned PEs, attenuating via D 2-like receptors the postsynaptic gain of sensory inputs forwarded by the auditory midbrain neurons. This direct dopaminergic modulation of sensory PE signaling has profound implications for both the predictive coding framework and the understanding of dopamine function.

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Section: Introductionmentioning

confidence: 99%

Dopamine modulates subcortical responses to surprising sounds

et al. 2020

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“…In the present study, we tested predictions of a popular model of hormone-dependent salience of courtship signals. 2,23,27,54,56,77 According to the model, reproductive hormones act on monoaminergic modulatory inputs to auditory areas, which themselves respond to external events and encode behavioural relevance.…”

Section: Discussionmentioning

confidence: 99%

Sound‐induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally‐breeding songbird

Rodríguez‐Saltos

Lyons

Sockman

et al. 2018

J Neuroendocrinology

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Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally-breeding female songbirds, for example, sound-induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma estradiol reaches breeding-like levels. This selectivity has been hypothesized to be mediated by release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen-primed female white-throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. In order to mediate hormone-dependent selectivity, this release must be (1) selective for song and (2) modulated by endocrine state. Therefore, in the current study we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or non-breeding endocrine state. We then used high performance liquid chromatography to measure turnover of dopamine, norepinephrine, and serotonin in the auditory midbrain and forebrain. We found that sound-induced turnover of dopamine and serotonin did in fact depend on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding-like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound-induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a non-breeding endocrine state. Our results suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated. This article is protected by copyright. All rights reserved.

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“…However, the neural mechanisms that promote the integration of experience and current context with sensory processing need more investigation. The central serotonergic system, situated mainly in the raphé nuclei, is a candidate mechanism by which information regarding both social history and current social context could be integrated with sensory processing (Petersen and Hurley 2017). The raphé nuclei are targeted by a diverse set of brain regions that relay different aspects of social information: primary sensory regions and higher order social centers, including nodes of the vertebrate social behavior network and regions important for processing reward (Goodson 2005;Pollak Dorocic et al 2014;Vertes and Linley 2008).…”

Section: Introductionmentioning

confidence: 99%

Social experience alters socially induced serotonergic fluctuations in the inferior colliculus

Keesom

Sloss

Erbowor-Becksen

et al. 2017

Journal of Neurophysiology

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Past social experience and current social context shape the responses of animals to social signals. The serotonergic system is one potential mechanism by which both experiential and contextual factors could be conveyed to sensory systems, such as the auditory system, for multiple reasons. ) Many features of the serotonergic system are sensitive to social experience.) Elevations in serotonergic activity are triggered by social partners, and variations in socially triggered serotonergic responses reflect behavioral differences among social encounters. ) Serotonin is an auditory neuromodulator, altering how auditory neurons respond to sounds including conspecific vocalizations. In this study, we tested how social experience influences the socially triggered serotonergic response in the inferior colliculus, an auditory midbrain region with an important role in vocalization processing. We used carbon fiber voltammetry to measure serotonin during social interactions of male mice () from different social backgrounds: 4 weeks of grouped or individual housing. When paired with an unfamiliar male, both group-housed and individually housed males demonstrated elevations in serotonin; however, individually housed males exhibited socially triggered serotonergic responses with delayed time courses compared with the group-housed males. Furthermore, group-housed males displayed previously described correlations between the socially triggered serotonergic response and behaviors such as social investigation. In contrast, individually housed males did not show these serotonin-behavior relationships. These results suggest that social experience gained via social housing may shape the ability of the central serotonergic system to encode social context in sensory regions. We demonstrate that past social experience influences the fidelity with which the serotonergic system represents social context in an auditory region. Social experience altered the time course of socially triggered serotonergic responses and changed how the serotonergic system reflects behavioral variations among social encounters of the same context. These findings are significant to the study of communication, suggesting that centralized neuromodulatory systems potentially convey integrated information regarding past experience and current context to primary sensory regions.

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Putting it in Context: Linking Auditory Processing with Social Behavior Circuits in the Vertebrate Brain

Cited by 20 publications

References 116 publications

Dopamine modulates subcortical responses to surprising sounds

Dopamine modulates subcortical responses to surprising sounds

Sound‐induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally‐breeding songbird

Social experience alters socially induced serotonergic fluctuations in the inferior colliculus

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