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

Rodríguez‐Saltos, Carlos A.; Lyons, Susan M.; Sockman, Keith W.; Maney, Donna L.

doi:10.1111/jne.12606

Cited by 11 publications

(6 citation statements)

References 74 publications

(215 reference statements)

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“…This finding led to the hypothesis that dopamine interacts with E2 signaling in NCM to support association learning. This line of reasoning is also supported by reports that dopamine in the auditory cortex mediates auditory association learning in gerbils (Schicknick et al, 2012), and that dopamine innervation and release are increased by steroid hormones in songbird NCM (Matragrano et al, 2011;Rodríguez-Saltos et al, 2018). In the present study, we provide anatomical evidence to support this hypothesis, since ~33% of aromatase+ neurons coexpress D1R protein and these co-labeled neurons represent ~8% of all 400 neurons in NCM (Fig.…”

Section: Discussionsupporting

confidence: 89%

Dopamine D1 receptor activation drives plasticity in the songbird auditory pallium

Macedo-Lima

Boyd

Remage‐Healey

2020

Preprint

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Vocal learning species must form and extensively hone associations between sounds and social contingencies. In songbirds, dopamine signaling guides song motor-production, variability, and motivation, but it is unclear how dopamine regulates fundamental auditory associations for learning new sounds. We hypothesized that dopamine regulates learning in the auditory pallium, in part by interacting with local neuroestradiol signaling. Here, we show that zebra finch auditory neurons frequently coexpress D1 receptor (D1R) protein, neuroestradiol-synthase, GABA, and parvalbumin. Auditory classical conditioning increased neuroplasticity gene induction in D1R-positive neurons. In vitro, D1R pharmacological activation reduced the amplitude of GABAergic and glutamatergic currents, and increased the latter’s frequency. In vivo, D1R activation reduced the firing of putative interneurons, increased the firing of putative excitatory neurons, and made both neuronal types unable to adapt to novel stimuli. Together, these data support the hypothesis that dopamine acting via D1Rs modulates learning and memory in the songbird sensory cortex.

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Section: Discussionsupporting

confidence: 89%

Dopamine D1 receptor activation drives plasticity in the songbird auditory pallium

Macedo-Lima

Boyd

Remage‐Healey

2020

Preprint

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“…The memories for tutor song that guide vocal imitation are thought to reside in the auditory forebrain 23,51 , a region rich in neuromodulators known to mediate social reward. Our own work with adult white-throated sparrows has shown that catecholaminergic activity increases in the auditory forebrain in females during sexual receptivity, when hearing song is likely rewarding 52,53 and that hearing song induces this activity further 54,55 . In young zebra finches, song learning may depend on catecholaminergic circuits; Katic et al found that activity in the locus coeruleus, the source of noradrenergic input to the auditory forebrain, increases during live song tutoring and blocking presynaptic signaling in the auditory forebrain interferes with song learning 56 .…”

Section: Potential Neural Mechanismsmentioning

confidence: 98%

Song preferences predict the quality of vocal learning in zebra finches

Rodríguez‐Saltos

Bhise

et al. 2023

Sci Rep

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In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we tested the hypothesis that during song learning, the reward value of hearing a particular song predicts the degree to which that song will ultimately be learned. We measured the early song preferences of young male zebra finches (Taeniopygia guttata) in an operant key-pressing assay; each of two keys was associated with a higher likelihood of playing the song of the father or that of another familiar adult (“neighbor”). To minimize the effects of exposure on learning, we implemented a novel reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the father’s song early during song learning, before actual singing occurs in this species. When they reached adulthood, all the birds copied the father’s song. The accuracy with which the father’s song was imitated was positively correlated with the peak strength of the preference for the father’s song during the sensitive period of song learning. Our results show that preference for the song of a chosen tutor, in this case the father, predicted vocal learning during development.

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“…Breeding songbirds display increased auditory response latency, which correlates with high estradiol levels, and an increase in the density of serotonin receptors in the main auditory pathway of birds ( Caras et al 2010 ; Matragrano et al 2012 ). In addition to an increase in the density of serotonin receptors, more serotonin has also been observed in the auditory forebrain of breeding songbirds compared to those in nonbreeding conditions ( Rodríguez-Saltos et al 2018 ). This suggests that serotonergic responses that modulate the latency, and thus sensitivity, of neurons in the auditory forebrain needed for behaviors specific to each season could in turn be regulated by endocrine signaling that reflects both reproductive and feeding state ( Hurley and Pollak 2005 ; Rodríguez-Saltos et al 2018 ).…”

Section: Contextualizing Through Our Frameworkmentioning

confidence: 99%

“…In addition to an increase in the density of serotonin receptors, more serotonin has also been observed in the auditory forebrain of breeding songbirds compared to those in nonbreeding conditions ( Rodríguez-Saltos et al 2018 ). This suggests that serotonergic responses that modulate the latency, and thus sensitivity, of neurons in the auditory forebrain needed for behaviors specific to each season could in turn be regulated by endocrine signaling that reflects both reproductive and feeding state ( Hurley and Pollak 2005 ; Rodríguez-Saltos et al 2018 ). In addition to changes in hormone levels, Miller et al also suggested that future research on the big brown bat could help us understand how changes in endocrine signaling, seasonal light/dark cycle, and temperature influence auditory plasticity in order to encode and integrate the availability of multiple needs.…”

Section: Contextualizing Through Our Frameworkmentioning

confidence: 99%

Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time

Kanwal

Coddington

Frazer

et al. 2021

Integrative and Comparative Biology

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Internal state profoundly alters perception and behavior. For example, a starved fly may approach and consume foods that it would otherwise find undesirable. A socially engaged newt may remain engaged in the presence of a predator, whereas a solitary newt would otherwise attempt escape. Yet, the definition of internal state is fluid and ill-defined. As an interdisciplinary group of scholars spanning five career stages (from undergraduate to full professor) and six academic institutions, we have come together in an attempt to provide an operational definition of internal state that could be useful in understanding behavior and the function of nervous systems, at timescales relevant to the individual. In this Perspective, we propose to define internal state through an integrative framework centered on dynamic and interconnected communication loops in and between the body and the brain. This framework is informed by a synthesis of historical and contemporary paradigms used by neurobiologists, ethologists, physiologists, and endocrinologists. We view internal state as composed of both spatially distributed networks (body-brain communication loops), and temporally distributed mechanisms that weave together neural circuits, physiology, and behavior. Given the wide spatial and temporal scales at which internal state operates—and therefore the broad range of scales at which it could be defined—we choose to anchor our definition in the body. Here we focus on studies that highlight body-to-brain signaling; body represented in endocrine signaling, and brain represented in sensory signaling. This integrative framework of internal state potentially unites the disparate paradigms often used by scientists grappling with body-brain interactions. We invite others to join us as we examine approaches and question assumptions to study the underlying mechanisms and temporal dynamics of internal state.

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

Cited by 11 publications

References 74 publications

Dopamine D1 receptor activation drives plasticity in the songbird auditory pallium

Dopamine D1 receptor activation drives plasticity in the songbird auditory pallium

Song preferences predict the quality of vocal learning in zebra finches

Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time

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