Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches.
Ontology highlight
ABSTRACT:
SUBMITTER: Benichov JI
PROVIDER: S-EPMC6954284 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Significance During conversations, we frequently alternate between listening and speaking. This involves withholding responses while the other person is vocalizing and rapidly initiating a reply once they stop. Similar exchanges also occur in other animals, such as songbirds, yet little is known about how brain areas responsible for vocal production are influenced by areas dedicated to listening. Here, we combined neural recordings and mathematical modeling of a sensorimotor circuit to show that input-dependent inhibition can both suppress vocal responses and regulate the onset latencies of vocalizations. Our resulting model provides a simple generalizable circuit mechanism by which inhibition precisely times vocal output and integrates auditory input within a premotor nucleus.
| S-EPMC9191632 | biostudies-literature
Project description:BACKGROUND: Birdsong and human vocal communication are both complex behaviours which show striking similarities mainly thought to be present in the area of development and learning. Recent studies, however, suggest that there are also parallels in vocal production mechanisms. While it has been long thought that vocal tract filtering, as it occurs in human speech, only plays a minor role in birdsong there is an increasing number of studies indicating the presence of sound filtering mechanisms in bird vocalizations as well. METHODOLOGY/PRINCIPAL FINDINGS: Correlating high-speed X-ray cinematographic imaging of singing zebra finches (Taeniopygia guttata) to song structures we identified beak gape and the expansion of the oropharyngeal-esophageal cavity (OEC) as potential articulators. We subsequently manipulated both structures in an experiment in which we played sound through the vocal tract of dead birds. Comparing acoustic input with acoustic output showed that OEC expansion causes an energy shift towards lower frequencies and an amplitude increase whereas a wide beak gape emphasizes frequencies around 5 kilohertz and above. CONCLUSION: These findings confirm that birds can modulate their song by using vocal tract filtering and demonstrate how OEC and beak gape contribute to this modulation.
| S-EPMC2912855 | biostudies-literature
Project description:Individual recognition is critical in social animal communication, but it has not been demonstrated for a complete vocal repertoire. Deciphering the nature of individual signatures across call types is necessary to understand how animals solve the problem of combining, in the same signal, information about identity and behavioral state. We show that distinct signatures differentiate zebra finch individuals for each call type. The distinctiveness of these signatures varies: contact calls bear strong individual signatures while calls used during aggressive encounters are less individualized. We propose that the costly solution of using multiple signatures evolved because of the limitations of the passive filtering properties of the birds' vocal organ for generating sufficiently individualized features. Thus, individual recognition requires the memorization of multiple signatures for the entire repertoire of conspecifics of interests. We show that zebra finches excel at these tasks.
| S-EPMC6168511 | biostudies-literature
Project description:Individuals with fragile X syndrome (FXS) are cognitively impaired and have marked speech delays and deficits. Our goal was to characterize expression of fragile X mental retardation protein (FMRP), encoded by Fmr1 fragile X mental retardation 1 gene or transcript (FMR1), in an animal model that learns to vocalize, namely the zebra finch Taeniopygia guttata (Tgu). We cloned and sequenced the zebra finch ortholog of FMR1 (TguFmr1) and developed an antibody that recognizes TguFmrp specifically. TguFmrp has structural features similar to its human ortholog FMRP. Because FXS patients exhibit sensorimotor deficits, we examined TguFmrp expression prior to, during, and after sensorimotor song learning in zebra finches. We found that TguFmrp is expressed throughout the brain and in four major song nuclei of the male zebra finch brain, primarily in neurons. Additionally, prior to sensorimotor learning, we observed elevated TguFmrp expression in the robust nucleus of the arcopallium (RA) of post-hatch day 30 males, compared with the surrounding telencephalon, suggesting a preparation for this stage of song learning. Finally, we observed variable TguFmrp expression in the RA of adolescent and adult males: in some males it was elevated and in others it was comparable to the surrounding telencephalon. In summary, we have characterized the zebra finch ortholog of FMRP and found elevated levels in the premotor nucleus RA at a key developmental stage for vocal learning.
| S-EPMC2598769 | biostudies-literature
Project description:In the vocal learning model, the juvenile first memorizes a model sound, and the imprinted memory gradually converts into vocal-motor output during the sensorimotor integration. However, early acquired memory may not precisely represent the fine structures of a model sound. How do juveniles ensure precise model imitation? Here we show that juvenile songbirds develop an auditory learning program by actively and attentively engaging with tutor's singing during the sensorimotor phase. The listening/approaching behavior requires previously acquired model memory and the individual variability of approaching behavior correlates with the precision of tutor song imitation. Moreover, it is modulated by dopamine and associated with forebrain regions for sensory processing. Overall, precise vocal learning may involve two steps of auditory processing: a passive imprinting of model memory occurs during the early sensory period; the previously acquired memory then guides an active and selective engagement of the re-exposed model to fine tune model imitation.
| S-EPMC8437935 | biostudies-literature
Project description:ObjectivesThe primary objective of the study was to examine the occurrence and temporal structure of vocal turn-taking during spontaneous interactions between mothers and their children with cochlear implants (CI) over the first year after cochlear implantation as compared with interactions between mothers and children with normal hearing (NH).DesignMothers' unstructured play sessions with children with CI (n = 12) were recorded at 2 time points, 3 months (mean age 18.3 months) and 9 months (mean age 27.5 months) post-CI. A separate control group of mothers with age-matched hearing children (n = 12) was recorded at the same 2 time points. Five types of events were coded: mother and child vocalizations, vocalizations including speech overlap, and between- and within-speaker pauses. We analyzed the proportion of child and mother vocalizations involved in turn-taking, the temporal structure of turn-taking, and the temporal reciprocity of turn-taking using proportions of simultaneous speech and the duration of between- and within-speaker pauses.ResultsThe CI group produced a significantly smaller proportion of vocalizations in turn-taking than the NH group at the first session; however, CI children's proportion of vocalizations in turn-taking increased over time. There was a significantly larger proportion of simultaneous speech in the CI compared with the NH group at the first session. The CI group produced longer between-speaker pauses as compared with those in the NH group at the first session with mothers decreasing the duration of between-speaker pauses over time. NH infants and mothers in both groups produced longer within- than between-speaker pauses but CI infants demonstrated the opposite pattern. In addition, the duration of mothers' between-speaker pauses (CI and NH) was predicted by the duration of the infants' between-speaker pauses.ConclusionsVocal turn-taking and timing in both members of the dyad, the mother and infant, were sensitive to the experiential effects of child hearing loss and remediation with CI. Child hearing status affected dyad-specific coordination in the timing of responses between mothers and their children.
| S-EPMC9618230 | biostudies-literature
Project description:Vocal imitation involves incorporating instructive auditory information into relevant motor circuits through processes that are poorly understood. In zebra finches, we found that exposure to a tutor's song drives spiking activity within premotor neurons in the juvenile, whereas inhibition suppresses such responses upon learning in adulthood. We measured inhibitory currents evoked by the tutor song throughout development while simultaneously quantifying each bird's learning trajectory. Surprisingly, we found that the maturation of synaptic inhibition onto premotor neurons is correlated with learning but not age. We used synthetic tutoring to demonstrate that inhibition is selective for specific song elements that have already been learned and not those still in refinement. Our results suggest that structured inhibition plays a crucial role during song acquisition, enabling a piece-by-piece mastery of complex tasks.
| S-EPMC4860291 | biostudies-other
Project description:Here we provide a detailed step-by-step protocol for using lentivirus to manipulate miRNA expression in Area X of juvenile zebra finches and for analyzing the consequences on song learning and song performance. This protocol has four parts: 1) making the lentiviral construct to overexpress miRNA miR-9; 2) packaging the lentiviral vector; 3) stereotaxic injection of the lentivirus into Area X of juvenile zebra finches; 4) analysis of song learning and song performance in juvenile and adult zebra finches. These methods complement the methods employed in recent works that showed changing FoxP2 gene expression in Area X with lentivirus or adeno-associated virus leads to impairments in song behavior.
| S-EPMC6261383 | biostudies-other
Project description:Neuromodulators can rapidly modify neural circuits, altering behavior. Songbirds provide an excellent system for studying the role of neuromodulation in modifying circuits that underlie behavior because song learning and production are mediated by a discrete set of interconnected nuclei. We examined the neuromodulatory effects of noradrenergic and GABA B receptor activation on synaptic inputs to the premotor robust nucleus of the arcopallium (RA) in zebra finches using whole cell voltage-clamp recording in vitro. In adults, norepinephrine strongly reduced input from the lateral magnocellular nucleus of the anterior nidopallium (LMAN) but only slightly reduced the input from nucleus HVC (proper name), the excitatory input from axon collaterals of other RA neurons, and input from GABAergic interneurons. The effect of norepinephrine was mimicked by the alpha2 adrenoceptor agonist UK14,304 and blocked by the alpha2 antagonist yohimbine. Conversely, the GABA B receptor agonist baclofen strongly decreased HVC, collateral, and GABAergic inputs to RA neurons while causing little reduction in the LMAN input. In juveniles undergoing song learning, norepinephrine reduced the LMAN input, caused only a small reduction in the HVC input, and greatly reduced the collateral and GABAergic inputs. Baclofen caused similar results in juvenile and adult birds, reducing HVC, collateral, and GABAergic inputs significantly more than the LMAN input. Significant increases in paired-pulse ratio accompanied all reductions in synaptic transmission, suggesting a presynaptic locus. The reduction in the LMAN input by norepinephrine may be important for mediating changes in song elicited by different social contexts and is well-placed to play a role in song learning.
| S-EPMC4071943 | biostudies-literature
Project description:In species with vocal learning, acquiring species-typical vocalizations relies on early social orienting. In songbirds, for example, learning song requires dynamic social interactions with a "tutor" during an early sensitive period. Here, we hypothesized that the attentional and motivational processes that support song learning recruit the oxytocin system, which is well-understood to play a role in social orienting in other species. Juvenile male zebra finches naïve to song were each tutored by two unfamiliar adult males. Before exposure to one tutor, juveniles were injected subcutaneously with oxytocin receptor antagonist (OTA; ornithine vasotocin) and before exposure to the other, saline (control). Treatment with OTA reduced behaviors associated with approach and attention during tutoring sessions. Using a novel operant paradigm to measure preference while balancing exposure to the two tutor songs, we showed that the juveniles preferred to hear the song of the control tutor. Their adult songs more closely resembled the control tutor's song, and the magnitude of this difference was predicted by early preference for control over OTA song. Overall, oxytocin antagonism during exposure to a tutor seemed to bias juveniles against that tutor and his song. Our results suggest that oxytocin receptors are important for socially-guided vocal learning.
| S-EPMC10185528 | biostudies-literature