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[This corrects the article DOI: 10.3389/fncir.2022.970434.].
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Recent studies conducted in the natural habitats of songbirds have provided new insights into the neural mechanisms of turn-taking. For example, female and male plain-tailed wrens (Pheugopedius euophrys) sing a duet that is so precisely timed it sounds as if a single bird is singing. In this review, we discuss our studies examining the sensory and motor cues that pairs of wrens use to coordinate the rapid alternation of syllable production. Our studies included behavioral measurements of freely-behaving wrens in their natural habitat and neurophysiological experiments conducted in awake and anesthetized individuals at field sites in Ecuador. These studies show that each partner has a pattern-generating circuit in their brain that is linked via acoustic feedback between individuals. A similar control strategy has been described in another species of duetting songbird, white-browed sparrow-weavers (Plocepasser mahali). Interestingly, the combination of neurophysiological results from urethane-anesthetized and awake wrens suggest a role for inhibition in coordinating the timing of turn-taking. Finally, we highlight some of the unique challenges of conducting these experiments at remote field sites.
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Pájaros Cantores , Vocalización Animal , Acústica , Animales , Encéfalo/fisiología , Femenino , Masculino , Pájaros Cantores/fisiología , Uretano , Vocalización Animal/fisiologíaRESUMEN
Widely used in research laboratories, immunohistochemistry (IHC) is a transferable skill that prepares undergraduate students for a variety of careers in the biomedical field. We have developed an inquiry-based learning IHC laboratory exercise, which introduces students to the theory, procedure, and data interpretation of antibody staining. Students are tasked with performing IHC using an "unknown" antibody and then asked to identify the cells or molecular structures within the nervous systems specific for that unknown antibody. In two lab sessions, students are exposed to handling of delicate brain slices, fluorescent microscopy, and data analysis using the Allen Brain Atlas (ABA), an online freely accessible database of mRNA transcript expression patterns in the brain. Here, we present guidelines for easy implementation in the classroom and assess learning gains achieved by the students upon completion of the IHC laboratory module. Students clearly displayed an increase in knowledge in data interpretation, procedural knowledge, and theory surrounding IHC. Thus, this module works as an inquiry-based learning based method to introduce IHC principles to undergraduate students.
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Laboratorios , Biología Molecular , Humanos , Inmunohistoquímica , Aprendizaje , Biología Molecular/educación , EstudiantesRESUMEN
The songs of mature zebra finches are notoriously repetitious, or 'crystallized'. Despite this stability, new work reveals that chronic pharmacologically driven bursting of cortical inputs to the basal ganglia can drive cumulative and lasting changes to multiple vocal features, including phenomena reminiscent of human stuttering.
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Pinzones , Animales , Ganglios Basales , Vocalización AnimalRESUMEN
Coordination of behavior for cooperative performances often relies on linkages mediated by sensory cues exchanged between participants. How neurophysiological responses to sensory information affect motor programs to coordinate behavior between individuals is not known. We investigated how plain-tailed wrens (Pheugopedius euophrys) use acoustic feedback to coordinate extraordinary duet performances in which females and males rapidly take turns singing. We made simultaneous neurophysiological recordings in a song control area "HVC" in pairs of singing wrens at a field site in Ecuador. HVC is a premotor area that integrates auditory feedback and is necessary for song production. We found that spiking activity of HVC neurons in each sex increased for production of its own syllables. In contrast, hearing sensory feedback produced by the bird's partner decreased HVC activity during duet singing, potentially coordinating HVC premotor activity in each bird through inhibition. When birds sang alone, HVC neurons in females but not males were inhibited by hearing the partner bird. When birds were anesthetized with urethane, which antagonizes GABAergic (γ-aminobutyric acid) transmission, HVC neurons were excited rather than inhibited, suggesting a role for GABA in the coordination of duet singing. These data suggest that HVC integrates information across partners during duets and that rapid turn taking may be mediated, in part, by inhibition.
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Pájaros Cantores/fisiología , Vocalización Animal/fisiología , Animales , Femenino , MasculinoRESUMEN
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.
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Percepción Auditiva/fisiología , Aves/fisiología , Vocalización Animal/fisiología , Comunicación Animal , Animales , Conducta Animal/fisiología , Femenino , Masculino , Matrimonio , Conducta Social , Pájaros CantoresRESUMEN
The evolutionary conservation of neural mechanisms for forming and maintaining pair bonds is unclear. Oxytocin, vasopressin and dopamine (DA) transmitter systems have been shown to be important in pair-bond formation and maintenance in several vertebrate species. We examined the role of dopamine in formation of song preference in zebra finches, a monogamous bird. Male courtship song is an honest signal of sexual fitness; thus, we measured female song preference to evaluate the role of DA in mate selection and pair-bond formation, using an operant conditioning paradigm. We found that DA acting through the D2 receptor, but not the D1 receptor, can induce a song preference in unpaired female finches and that blocking the D2 receptor abolished song preference in paired females. These results suggest that similar neural mechanisms for pair-bond formation are evolutionarily conserved in rodents and birds.
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Proteínas Aviares/genética , Cortejo , Dopamina/metabolismo , Receptores de Dopamina D1/genética , Receptores de Dopamina D2/genética , Pájaros Cantores/fisiología , Vocalización Animal , Animales , Proteínas Aviares/metabolismo , Condicionamiento Operante , Femenino , Pinzones/fisiología , Receptores de Dopamina D1/metabolismo , Receptores de Dopamina D2/metabolismoRESUMEN
An operant conditioning paradigm is used to test the song preference of female zebra finches. Finches are placed in a two-chambered cage with a connecting opening and indicate their preference for a song by landing on a perch within each chamber. By interrupting the infrared beam from a photoelectric sensor above each perch, the bird activates the playback of a song through a speaker located on each side of the cage. Freely available software is used to trigger the song playback from each perch. To determine the song preference of each animal, her chamber preference is first identified by triggering no song playback when she lands on each perch. This chamber preference is then compared to her song preference. A minimum activity threshold is set to ensure the preference is real. Using this method, we show that paired females prefer the song of their partner. This method was used to understand the contribution of dopamine to the formation and maintenance of song preference.
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Condicionamiento Operante , Pinzones/fisiología , Vocalización Animal/fisiología , Animales , Dopamina/fisiología , Femenino , MasculinoRESUMEN
Behavioral variability is thought to be critical for trial and error learning, but where such motor exploration is generated in the central nervous system is unclear. The zebra finch songbird species offers a highly appropriate model in which to address this question. The male song is amenable to detailed measurements of variability, while the brain contains an identified cortico-basal ganglia loop that underlies this behavior. We used pharmacogenetic interventions to separately interrogate cortical and basal ganglia nodes of zebra finch song control circuitry. We show that bidirectional manipulations of each node produce near mirror image changes in vocal control: Cortical activity promotes song variability, whereas basal ganglia activity promotes song stability. Furthermore, female conspecifics can detect these pharmacogenetically elicited changes in song quality. Our results indicate that cortex and striatopallidum can jointly and reciprocally affect behaviorally relevant levels of vocal variability, and point to endogenous mechanisms for its control.
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Ganglios Basales/fisiología , Corteza Cerebral/fisiología , Pinzones/fisiología , Aprendizaje/fisiología , Vocalización Animal/fisiología , Estimulación Acústica , Animales , Masculino , Vías Nerviosas/fisiología , FarmacogenéticaRESUMEN
Birdsong is a learned behavior that is controlled by a group of identified nuclei, known collectively as the song system. The cortical nucleus HVC (used as a proper name) is a focal point of many investigations as it is necessary for song production, song learning, and receives selective auditory information. HVC receives input from several sources including the cortical area MMAN (medial magnocellular nucleus of the nidopallium). The MMAN to HVC connection is particularly interesting as it provides potential sensorimotor feedback to HVC. To begin to understand the role of this connection, we investigated the physiological relation between MMAN and HVC activity with simultaneous multiunit extracellular recordings from these two nuclei in urethane anesthetized zebra finches. As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC. Like HVC, MMAN responds to auditory playback of the bird's own song (BOS), but had little response to reversed BOS or conspecific song. Stimulation of MMAN resulted in evoked activity in HVC, indicating functional excitation from MMAN to HVC. However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC. Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals. We hypothesize that MMAN may play a role in motor reinforcement or coordination, or may provide modulatory input to the song system about the internal state of the animal as it receives input from the hypothalamus.
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Retroalimentación Sensorial , Pinzones/fisiología , Sinapsis/fisiología , Estimulación Acústica/métodos , Potenciales de Acción , Animales , Vías Auditivas/fisiología , Electrofisiología/métodos , Hipotálamo/fisiología , Masculino , Modelos Biológicos , Modelos Estadísticos , Pájaros Cantores , Vocalización Animal/fisiologíaRESUMEN
Plain-tailed wrens (Pheugopedius euophrys) cooperate to produce a duet song in which males and females rapidly alternate singing syllables. We examined how sensory information from each wren is used to coordinate singing between individuals for the production of this cooperative behavior. Previous findings in nonduetting songbird species suggest that premotor circuits should encode each bird's own contribution to the duet. In contrast, we find that both male and female wrens encode the combined cooperative output of the pair of birds. Further, behavior and neurophysiology show that both sexes coordinate the timing of their singing based on feedback from the partner and suggest that females may lead the duet.
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Neuronas/fisiología , Pájaros Cantores/fisiología , Animales , Femenino , Masculino , Vocalización Animal/fisiologíaRESUMEN
Higher cognitive function depends on accurate detection and processing of subtle features of sensory stimuli. Such precise computations require neural circuits to be modulated over rapid timescales, yet this modulation is poorly understood. Brain-derived steroids (neurosteroids) can act as fast signaling molecules in the vertebrate central nervous system and could therefore modulate sensory processing and guide behavior, but there is no empirical evidence for this possibility. Here we report that acute inhibition of estrogen production within a cortical-like region involved in complex auditory processing disrupts a songbird's ability to behaviorally respond to song stimuli. Identical manipulation of local estrogen levels rapidly changes burst firing of single auditory neurons. This acute estrogen-mediated modulation targets song and not other auditory stimuli, possibly enabling discrimination among species-specific signals. Our results demonstrate a crucial role for neuroestrogen synthesis among vertebrates for enhanced sensory encoding. Cognitive impairments associated with estrogen depletion, including verbal memory loss in humans, may therefore stem from compromised moment-by-moment estrogen actions in higher-order cortical circuits.
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Percepción Auditiva/fisiología , Encéfalo/fisiología , Cognición/fisiología , Estrógenos/fisiología , Pinzones/fisiología , Vocalización Animal/fisiología , Estimulación Acústica , Animales , Aromatasa/fisiología , Encéfalo/metabolismo , Estrógenos/biosíntesis , Estrógenos/deficiencia , MasculinoRESUMEN
Songbirds learn to sing by memorizing a tutor song that they then vocally mimic using auditory feedback. This developmental sequence suggests that brain areas that encode auditory memories communicate with brain areas for learned vocal control. In the songbird, the secondary auditory telencephalic region caudal mesopallium (CM) contains neurons that encode aspects of auditory experience. We investigated whether CM is an important source of auditory input to two sensorimotor structures implicated in singing, the telencephalic song nucleus interface (NIf) and HVC. We used reversible inactivation methods to show that activity in CM is necessary for much of the auditory-evoked activity that can be detected in NIf and HVC of anesthetized adult male zebra finches. Furthermore, extracellular and intracellular recordings along with spike-triggered averaging methods indicate that auditory selectivity for the bird's own song is enhanced between CM and NIf. We used lentiviral-mediated tracing methods to confirm that CM neurons directly innervate NIf. To our surprise, these tracing studies also revealed a direct projection from CM to HVC. We combined irreversible lesions of NIf with reversible inactivation of CM to establish that CM supplies a direct source of auditory drive to HVC. Finally, using chronic recording methods, we found that CM neurons are active in response to song playback and during singing, indicating their potential importance to song perception and processing of auditory feedback. These results establish the functional synaptic linkage between sites of auditory and vocal learning and may identify an important substrate for learned vocal communication.
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Vías Auditivas/fisiología , Percepción Auditiva/fisiología , Pájaros Cantores/fisiología , Sinapsis/fisiología , Vocalización Animal/fisiología , Estimulación Acústica/métodos , Animales , Pinzones , MasculinoRESUMEN
In songbirds, nucleus Uvaeformis (Uva) is the sole thalamic input to the telencephalic nucleus HVC (used as a proper name), a sensorimotor structure essential to learned song production that also exhibits state-dependent responses to auditory presentation of the bird's own song (BOS). The role of Uva in influencing HVC auditory activity is unknown. Using in vivo extracellular and intracellular recordings in urethane-anesthetized zebra finches, we characterized the auditory properties of Uva and examined its influence on auditory activity in HVC and in the telencephalic nucleus interface (NIf), the main auditory afferent of HVC and a corecipient of Uva input. We found robust auditory activity in Uva and determined that Uva is innervated by the ventral nucleus of lateral lemniscus, an auditory brainstem component. Thus, Uva provides a direct linkage between the auditory brainstem and HVC. Although low-frequency electrical stimulation in Uva elicited short-latency depolarizing postsynaptic potentials in HVC neurons, reversibly silencing Uva exerted little effect on BOS-evoked activity in HVC neurons. However, high-frequency stimulation in Uva suppressed auditory-evoked synaptic and suprathreshold activity in all HVC neuron types, a process accompanied by decreased input resistance of individual HVC neurons. Furthermore, high-frequency stimulation in Uva simultaneously suppressed auditory activity in HVC and NIf. These results suggest that Uva can gate auditory responses in HVC through a mechanism that involves inhibition local to HVC as well as withdrawal of auditory-evoked excitatory drive from NIf. Thus, Uva could play an important role in state-dependent gating of auditory activity in telencephalic sensorimotor structures important to learned vocal control.
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Vías Auditivas/fisiología , Telencéfalo/fisiología , Tálamo/fisiología , Vocalización Animal/fisiología , Estimulación Acústica/métodos , Potenciales de Acción/fisiología , Animales , Femenino , Pinzones , Masculino , Pájaros CantoresRESUMEN
Zebra finches utilize neural circuits in both cerebral hemispheres to produce their learned songs. Although direct reciprocal connections do not exist between song control nuclei across hemispheres, premotor activity in these nuclei during singing is precisely and continuously coordinated between the hemispheres. We hypothesized that this interhemispheric coordination is mediated by bilateral feedback projections from medullary and midbrain song control nuclei to the thalamic song control nucleus uvaeformis (Uva). Consistent with our hypothesis, bilateral lesions of Uva severely impaired singing. This impairment was long-lasting, as it persisted for at least 35 days after the lesions. Unilateral lesions of Uva on either side also resulted in an immediate singing impairment. However, song recovered substantially after less than 15 days, suggesting a possible compensation by the unlesioned side. Although the acoustic structure of individual syllables recovered fully after unilateral lesioning, subtle changes in the sequencing of syllables were observed after song recovery, suggesting that the lesion led to an alteration in the functioning of the remaining song control network. These results demonstrate that the adult songbird brain can adjust to damage to certain parts of the song control network and recover from their associated singing deficits. The well-identified and localized central neural pathways mediating birdsong production provide an advantageous model system to analyze systematically the sensorimotor contexts and the specific sites and mechanisms for behavioral recovery following partial damage to a behavior-producing neural circuit.
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Lateralidad Funcional/fisiología , Núcleos Talámicos Posteriores/fisiología , Recuperación de la Función/fisiología , Vocalización Animal/fisiología , Animales , Conducta Animal , Encefalopatías/fisiopatología , Retroalimentación , Femenino , Pinzones , Masculino , Vías Nerviosas/fisiología , Núcleos Talámicos Posteriores/lesiones , Espectrografía del Sonido , Factores de TiempoRESUMEN
Stimulus-specific neuronal responses are a striking characteristic of several sensory systems, although the synaptic mechanisms underlying their generation are not well understood. The songbird nucleus HVC (used here as a proper name) contains projection neurons (PNs) that fire temporally sparse bursts of action potentials to playback of the bird's own song (BOS) but are essentially silent when presented with other acoustical stimuli. To understand how such remarkable stimulus specificity emerges, it is necessary to compare the auditory-evoked responsiveness of the afferents of HVC with synaptic responses in identified HVC neurons. We found that inactivating the interfacial nucleus of the nidopallium (NIf) could eliminate all auditory-evoked subthreshold activity in both HVC PN types, consistent with NIf serving as the major auditory afferent of HVC. Simultaneous multiunit extracellular recordings in NIf and intracellular recordings in HVC revealed that NIf population activity and HVC subthreshold responses were similar in their selectivity for BOS and that NIf spikes preceded depolarizations in all HVC cell types. These results indicate that information about the BOS as well as other auditory stimuli is transmitted synaptically from NIf to HVC. Unlike HVC PNs, however, HVC-projecting NIf neurons fire throughout playback of BOS as well as non-BOS stimuli. Therefore, temporally sparse BOS-evoked firing and enhanced BOS selectivity, manifested as an absence of suprathreshold responsiveness to non-BOS stimuli, emerge in HVC. The transformation to a sparse auditory representation parallels differences in NIf and HVC activity patterns seen during singing, which may point to a common mechanism for encoding sensory and motor representations of song.
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Neuronas Aferentes/fisiología , Pájaros Cantores/fisiología , Transmisión Sináptica , Telencéfalo/fisiología , Vocalización Animal/fisiología , Animales , Vías Auditivas , Potenciales Evocados Auditivos , Aprendizaje , Masculino , Potenciales de la Membrana , Telencéfalo/citologíaRESUMEN
The ability of calcium/calmodulin-dependent protein kinase II (CaMKII) to become calcium independent after autophosphorylation makes this enzyme a temporal marker of neuronal activity. Here we show that the calcium-independent form of CaMKII has unique effects on larval viability, locomotion, and neuronal excitability in Drosophila. Expression of constitutively active T287D, but not calcium-dependent T287A, mutant CaMKII in Drosophila neurons resulted in decreased viability, behavioral defects, and failure of action potential propagation. The actions of T287D may be mediated, at least in part, by increased potassium conductances. Expression of T287D CaMKII also stimulated an increase in the number of boutons at the larval neuromuscular junction, but did not affect the mechanics of release. This study defines a role for autophosphorylation of CaMKII in the regulation of multiple neuronal functions including the intrinsic properties of neurons.