scholarly journals Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches

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.

The Condor ◽  
2006 ◽  
Vol 108 (2) ◽  
pp. 326-335 ◽  
Author(s):  
David M. Logue

Abstract In many duet-singing songbirds, paired birds combine their song types nonrandomly to form duet songs. Several different behavioral mechanisms could generate nonrandom song type associations in duets. I tested female Black-bellied Wrens (Thryothorus fasciatoventris) for one such mechanism: adherence to a set of rules linking female response songs to male stimulus songs. I call this set of rules a “duet code.” Duets of free-living Black-bellied Wrens were recorded in 2001 and 2002. In 2003 I returned to the same territories and played the male song types from the recorded duets. Females answered male song stimuli as if duetting with the playback speaker. Although the known repertoires of females averaged 8.4 song types, each female sang only a single song type in response to each male song type. Random answering could not account for this pattern, supporting the hypothesis that females abide by duet codes. Females that were still paired with their mates from 2001–2002 answered 100% of their mate's songs with the same song types they had used previously, demonstrating that codes are stable over time. In contrast, females that were new to a territory answered an average of only 18% of their mate's song types with the same song type as the previous female, indicating that duet codes are individually distinctive. Duet participation by female Black-bellied Wrens represents a special kind of animal communication, in which discrete vocal signals consistently elicit discrete vocal responses according to an individually distinctive set of rules.


eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Lisa F Gill ◽  
Wolfgang Goymann ◽  
Andries Ter Maat ◽  
Manfred Gahr

Vocal signals such as calls play a crucial role for survival and successful reproduction, especially in group-living animals. However, call interactions and call dynamics within groups remain largely unexplored because their relation to relevant contexts or life-history stages could not be studied with individual-level resolution. Using on-bird microphone transmitters, we recorded the vocalisations of individual zebra finches (Taeniopygia guttata) behaving freely in social groups, while females and males previously unknown to each other passed through different stages of the breeding cycle. As birds formed pairs and shifted their reproductive status, their call repertoire composition changed. The recordings revealed that calls occurred non-randomly in fine-tuned vocal interactions and decreased within groups while pair-specific patterns emerged. Call-type combinations of vocal interactions changed within pairs and were associated with successful egg-laying, highlighting a potential fitness relevance of calling dynamics in communication systems.


2020 ◽  
Vol 287 (1935) ◽  
pp. 20201884
Author(s):  
Elisa Castaldi ◽  
David Burr ◽  
Marco Turi ◽  
Paola Binda

Fast saccades are rapid automatic oculomotor responses to salient and ecologically important visual stimuli such as animals and faces. Discriminating the number of friends, foe, or prey may also have an evolutionary advantage. In this study, participants were asked to saccade rapidly towards the more numerous of two arrays. Participants could discriminate numerosities with high accuracy and great speed, as fast as 190 ms. Intermediate numerosities were more likely to elicit fast saccades than very low or very high numerosities. Reaction-times for vocal responses (collected in a separate experiment) were slower, did not depend on numerical range, and correlated only with the slow not the fast saccades, pointing to different systems. The short saccadic reaction-times we observe are surprising given that discrimination using numerosity estimation is thought to require a relatively complex neural circuit, with several relays of information through the parietal and prefrontal cortex. Our results suggest that fast numerosity-driven saccades may be generated on a single feed-forward pass of information recruiting a primitive system that cuts through the cortical hierarchy and rapidly transforms the numerosity information into a saccade command.


Author(s):  
Chongyang Sun ◽  
Yi Cao ◽  
Jianyu Huang ◽  
Kang Huang ◽  
Yi Lu ◽  
...  

Abstract Objective. Extracellular electrophysiology has been widely applied to neural circuit dissections. However, long-term multiregional recording in free-moving mice remains a challenge. Low-cost and easy-fabrication of elaborate drivable electrodes is required for their prevalence. Approach. A three-layer nested construct (OD ~1.80 mm, length ~10 mm, <0.1g) was recruited as a drivable component, which consisted of an ethylene-vinyl acetate copolymer (EVA) heat-shrinkable tube, non-closed loop ceramic bushing, and stainless ferrule with a bulge twining silver wire. The supporting and working components were equipped with drivable components to be assembled into a drivable microwire electrode array with a nested structure (drivable MEANS). Two drivable microwire electrode arrays were independently implanted for chronic recording in different brain areas at respective angles. An optic fiber was easily loaded into the drivable MEANS to achieve optogenetic modulation and electrophysiological recording simultaneously. Main results. The drivable MEANS had lightweight (~ 0.37 g), small (~ 15 mm ×15 mm × 4 mm), and low cost (≤ $64.62). Two drivable MEANS were simultaneously implanted in mice, and high-quality electrophysiological recordings could be applied ≥ 5 months after implantation in freely behaving animals. Electrophysiological recordings and analysis of the lateral septum (LS) and lateral hypothalamus (LH) in food-seeking behavior demonstrated that our drivable MEANS can be used to dissect the function of neural circuits. An optical fiber-integrated drivable MEANS (~ 0.47 g) was used to stimulate and record LS neurons, which suggested that changes in working components can achieve more functions than electrophysiological recordings, such as optical stimulation, drug release, and calcium imaging. Significance. Drivable MEANS is an easily fabricated, lightweight drivable microwire electrode array for multiple-region electrophysiological recording in free-moving mice. Our design is likely to be a valuable platform for both current and prospective users, as well as for developers of multifunctional electrodes for free-moving mice.


2018 ◽  
Author(s):  
Zheng Zhou ◽  
Xuemei Liu ◽  
Shanping Chen ◽  
Zhijian Zhang ◽  
Yu-anming Liu ◽  
...  

SUMMARYInnate defensive responses are essential for animal survival and are conserved across species. The ventral tegmental area (VTA) plays important roles in learned appetitive and aversive behaviors, but whether it plays a role in mediating or modulating innate defensive responses is currently unknown. We report that GABAergic neurons in the mouse VTA (VTAGABA+) are preferentially activated compared to VTA dopaminergic (VTADA+) neurons when a threatening visual stimulus evokes innate defensive behavior. Functional manipulation of these neurons showed that activation of VTAGABA+ neurons is indispensable for looming-evoked defensive flight behavior and photoactivation of these neurons is sufficient for looming-evoked defensive-like flight behavior, whereas no such role can be attributed for VTADA+ neurons. Viral tracing and in vivo and in vitro electrophysiological recordings showed that VTAGABA+ neurons receive direct excitatory inputs from the superior colliculus (SC). Furthermore, we showed that glutamatergic SC-VTA projections synapse onto VTAGABA+ neurons that project to the central nucleus of the amygdala (CeA) and that the CeA is involved in mediating the defensive behavior. Our findings demonstrate that visual information about aerial threats access to the VTAGABA+ neurons mediating innate behavioral responses, suggesting a more general role for the VTA.


2021 ◽  
Vol 224 (9) ◽  
Author(s):  
Marine Banse ◽  
Boris P. Chagnaud ◽  
Alessia Huby ◽  
Eric Parmentier ◽  
Loïc Kéver

ABSTRACT In piranhas, sounds are produced through the vibration of the swim bladder wall caused by the contraction of bilateral sonic muscles. Because they are solely innervated by spinal nerves, these muscles likely evolved from the locomotor hypaxial musculature. The transition from a neuromuscular system initially shaped for slow movements (locomotion) to a system that requires a high contraction rate (sound production) was accompanied with major peripheral structural modifications, yet the associated neural adjustments remain to this date unclear. To close this gap, we investigated the activity of both the locomotor and the sonic musculature using electromyography. The comparison between the activation patterns of both systems highlighted modifications of the neural motor pathway: (1) a transition from a bilateral alternating pattern to a synchronous activation pattern, (2) a switch from a slow- to a high-frequency regime, and (3) an increase in the synchrony of motor neuron activation. Furthermore, our results demonstrate that sound features correspond to the activity of the sonic muscles, as both the variation patterns of periods and amplitudes of sounds highly correspond to those seen in the sonic muscle electromyograms (EMGsonic). Assuming that the premotor network for sound production in piranhas is of spinal origin, our results show that the neural circuit associated with spinal motor neurons transitioned from the slow alternating pattern originally used for locomotion to a much faster simultaneous activation pattern to generate vocal signals.


2018 ◽  
Vol 5 (2) ◽  
pp. 171791 ◽  
Author(s):  
Karla D. Rivera-Cáceres ◽  
Esmeralda Quirós-Guerrero ◽  
Marcelo Araya-Salas ◽  
Christopher N. Templeton ◽  
William A. Searcy

Exchange of vocal signals is an important aspect of animal communication. Although birdsong is the premier model for understanding vocal development, the development of vocal interaction rules in birds and possible parallels to humans have been little studied. Many tropical songbirds engage in complex vocal interactions in the form of duets between mated pairs. In some species, duets show precise temporal coordination and follow rules (duet codes) governing which song type one bird uses to reply to each of the song types of its mate. We determined whether these duetting rules are acquired during early development in canebrake wrens. Results show that juveniles acquire a duet code by singing with a mated pair of adults and that juveniles gradually increase their fidelity to the code over time. Additionally, we found that juveniles exhibit poorer temporal coordination than adults and improve their coordination as time progresses. Human turn-taking, an analogous rule to temporal coordination, is learned during early development. We report that the ontogeny of vocal interaction rules in songbirds is analogous to that of human conversation rules.


2021 ◽  
Author(s):  
Silvana Valtcheva ◽  
Habon A. Issa ◽  
Kathleen A. Martin ◽  
Kanghoon Jung ◽  
Hyung-Bae Kwon ◽  
...  

SummaryOxytocin is a neuropeptide important for maternal physiology and childcare, including parturition and milk ejection during nursing. Suckling triggers oxytocin release, but other sensory cues- specifically infant cries- can elevate oxytocin levels in new human mothers, indicating that cries can activate hypothalamic oxytocin neurons. Here we describe a neural circuit routing auditory information about infant vocalizations to the oxytocin system of the mouse brain. We performed in vivo electrophysiological recordings and photometry from identified oxytocin neurons in awake maternal mice presented with pup calls. We found that oxytocin neurons responded to pup vocalizations via input from the posterior intralaminar thalamus, and repetitive thalamic stimulation induced lasting disinhibition of oxytocin neurons. Suppression of this pathway impaired maternal behavior and playing pup calls led to central oxytocin release in vivo. This circuit provides a mechanism for transforming acoustic input into hormonal output to ensure modulation of brain state required for successful parenting.


2010 ◽  
Vol 104 (6) ◽  
pp. 3180-3188 ◽  
Author(s):  
H. Neumeister ◽  
K. W. Whitaker ◽  
H. A. Hofmann ◽  
T. Preuss

Ecological context, sensory inputs, and the internal physiological state are all factors that need to be integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between two phenotypes based on position in a social hierarchy. When dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behavioral patterns that make them conspicuous to predators. Subordinate (SUB) males, on the other hand, decrease predation risk by adopting cryptic coloration and schooling behavior. We therefore hypothesized that DOMs would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs compared with SUBs. Electrophysiological recordings from the Mauthner cells (M-cells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons (passive hyperpolarizing potential [PHP] cells) presynaptic to the M-cell was significantly reduced in DOMs. Taken together, the results suggest that the likelihood for an escape to occur for a given auditory stimulus is higher in DOMs because of a more excitable M-cell. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit.


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