scholarly journals Dopamine depletion affects vocal acoustics and disrupts sensorimotor adaptation in songbirds

2019 ◽  
Author(s):  
Varun Saravanan ◽  
Lukas A Hoffmann ◽  
Amanda L Jacob ◽  
Gordon J Berman ◽  
Samuel J Sober

AbstractDopamine is hypothesized to convey important error information in reinforcement learning tasks with explicit appetitive or aversive cues. However, during motor skill learning the only available feedback signal is typically an animal’s evaluation of the sensory feedback arising from its own behavior, rather than any external reward or punishment. It has previously been shown that intact dopaminergic signaling from the ventral tegmental area – substantia nigra compacta complex (VTA/SNc) is necessary for vocal learning in response to an external aversive auditory cue in songbirds. However, the role of dopamine in learning in the absence of explicit external cues is still unclear. Here we used male Bengalese finches (Lonchura striatavar.domestica) to test the hypothesis that dopamine signaling is necessary for self-evaluation driven sensorimotor learning. We combined 6-hydroxydopamine (6-OHDA) lesions of dopaminergic terminals within Area X, a songbird basal ganglia nucleus critical for vocal learning, with a headphones learning paradigm that shifted the birds’ auditory feedback and compared their learning to birds without lesions. We found that 6-OHDA lesions affected song behavior in two ways. First, over a period of days lesioned birds systemically lowered their pitch regardless of the presence or absence of auditory errors. Second, 6-OHDA lesioned birds also displayed severe deficits in sensorimotor learning as measured by their adaptive change in pitch in response to the pitch-shifted auditory error. Our results suggest roles for dopamine both in motor production and in auditory error processing during vocal learning.Significance StatementDopamine has been hypothesized to convey a reward prediction error signal in learning tasks involving external reinforcement. However the role dopamine plays in tasks involving self-guided error correction in the absence of external reinforcement is much less clear. To address this question, we studied the role of dopamine in sensorimotor adaptation using male Bengalese finches, which spontaneously produce a complex motor behavior (song) and are capable of modulating their behavioral output in response to induced auditory errors. Our results reveal that in addition to conveying errors in motor performance, dopamine may also have a role in modulating effort and in choosing a corrective response to the auditory error.

2020 ◽  
Author(s):  
Yang Liu ◽  
Hannah J. Block

AbstractMotor skill learning involves both sensorimotor adaptation (calibrating the response to task dynamics and kinematics), and sequence learning (executing the task elements in the correct order at the necessary speed). These processes typically occur together in natural behavior and share much in common, such as working memory demands, development, and possibly neural substrates. However, sensorimotor and sequence learning are usually studied in isolation in research settings, for example as force field adaptation or serial reaction time tasks (SRTT), respectively. It is therefore unclear whether having predictive sequence information during sensorimotor adaptation would facilitate performance, perhaps by improving sensorimotor planning, or if it would impair performance, perhaps by occupying neural resources needed for sensorimotor learning. Here we evaluated adaptation to a distance-dependent force field in two different SRTT contexts: In Experiment 1, 28 subjects reached between 4 targets in a sequenced or random order. In Experiment 2, 40 subjects reached to one target, but 3 force field directions were applied in a sequenced or random order. We did not observe any consistent influence of target position sequence on force field adaptation in Experiment 1. However, sequencing of force field directions facilitated sensorimotor adaptation and retention in Experiment 2. This is inconsistent with the idea that sensorimotor and sequence learning share neural resources in any mutually exclusive fashion. These findings indicate that under certain conditions, perhaps especially when the sequence is related to the sensorimotor perturbation itself as in Experiment 2, sequence learning may interact with sensorimotor learning in a facilitatory manner.


2021 ◽  
pp. 1-14
Author(s):  
Claudia Cornelis ◽  
Livia J. De Picker ◽  
Violette Coppens ◽  
Anne Morsel ◽  
Maarten Timmers ◽  
...  

<b><i>Background:</i></b> The “cognitive dysmetria hypothesis” of schizophrenia proposes a disrupted communication between the cerebellum and cerebral cortex, resulting in sensorimotor and cognitive symptoms. Sensorimotor adaptation relies strongly on the function of the cerebellum. <b><i>Objectives:</i></b> This study investigated whether sensorimotor adaptation is reduced in schizophrenia compared with age-matched and elderly healthy controls. <b><i>Methods:</i></b> Twenty-nine stably treated patients with schizophrenia, 30 age-matched, and 30 elderly controls were tested in three motor adaptation tasks in which visual movement feedback was unexpectedly altered. In the “rotation adaptation task” the perturbation consisted of a rotation (30° clockwise), in the “gain adaptation task” the extent of the movement feedback was reduced (by a factor of 0.7) and in the “vertical reversal task,” up- and downward pen movements were reversed by 180°. <b><i>Results:</i></b> Patients with schizophrenia adapted to the perturbations, but their movement times and errors were substantially larger than controls. Unexpectedly, the magnitude of adaptation was significantly smaller in schizophrenia than elderly participants. The impairment already occurred during the first adaptation trials, pointing to a decline in explicit strategy use. Additionally, post-adaptation aftereffects provided strong evidence for impaired implicit adaptation learning. Both negative and positive schizophrenia symptom severities were correlated with indices of the amount of adaptation and its aftereffects. <b><i>Conclusions:</i></b> Both explicit and implicit components of sensorimotor adaptation learning were reduced in patients with schizophrenia, adding to the evidence for a role of the cerebellum in the pathophysiology of schizophrenia. Elderly individuals outperformed schizophrenia patients in the adaptation learning tasks.


2000 ◽  
Vol 84 (3) ◽  
pp. 1204-1223 ◽  
Author(s):  
Todd W. Troyer ◽  
Allison J. Doupe

Birdsong learning provides an ideal model system for studying temporally complex motor behavior. Guided by the well-characterized functional anatomy of the song system, we have constructed a computational model of the sensorimotor phase of song learning. Our model uses simple Hebbian and reinforcement learning rules and demonstrates the plausibility of a detailed set of hypotheses concerning sensory-motor interactions during song learning. The model focuses on the motor nuclei HVc and robust nucleus of the archistriatum (RA) of zebra finches and incorporates the long-standing hypothesis that a series of song nuclei, the Anterior Forebrain Pathway (AFP), plays an important role in comparing the bird's own vocalizations with a previously memorized song, or “template.” This “AFP comparison hypothesis” is challenged by the significant delay that would be experienced by presumptive auditory feedback signals processed in the AFP. We propose that the AFP does not directly evaluate auditory feedback, but instead, receives an internally generated prediction of the feedback signal corresponding to each vocal gesture, or song “syllable.” This prediction, or “efference copy,” is learned in HVc by associating premotor activity in RA-projecting HVc neurons with the resulting auditory feedback registered within AFP-projecting HVc neurons. We also demonstrate how negative feedback “adaptation” can be used to separate sensory and motor signals within HVc. The model predicts that motor signals recorded in the AFP during singing carry sensory information and that the primary role for auditory feedback during song learning is to maintain an accurate efference copy. The simplicity of the model suggests that associational efference copy learning may be a common strategy for overcoming feedback delay during sensorimotor learning.


2017 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Leblanc ◽  
Arthur Leblois

AbstractSpeech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Le Blanc ◽  
Carole Levenes ◽  
Arthur Leblois

Speech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.


Author(s):  
Jonathan Sanching Tsay ◽  
Hyosub E. Kim ◽  
Darius E. Parvin ◽  
Alissa R Stover ◽  
Richard B. Ivry

Recent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (visually biased) sensed hand position realigns with the expected sensed position (target). When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor, and the adaptive system counteracts this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior.


2012 ◽  
Vol 7 (1) ◽  
pp. 27-51 ◽  
Author(s):  
Susan L. Swanger ◽  
Beth H. Jones

ABSTRACT Accounting educators strive to prepare graduates for work in their chosen field. Various teaching methods can be employed to best accomplish this goal. One valuable tool is the use of active learning tasks that simulate external work environments. This paper describes the collaboration between an AIS and an Auditing professor who used an integrative task that spanned their two classes over two semesters. The authors had their AIS students complete Arens and Ward's Systems Understanding Aid (SUA) project (Arens & Ward, 2008). The following semester, students in the auditing class audited the records and financials that had been generated by students the previous semester. The project was designed to facilitate course integration and teamwork by having groups of students play the role of corporate accountants, then act as independent auditors.


2021 ◽  
Vol 11 (6) ◽  
pp. 681
Author(s):  
Alessia Bocchi ◽  
Massimiliano Palmiero ◽  
Jose Manuel Cimadevilla Redondo ◽  
Laura Tascón ◽  
Raffaella Nori ◽  
...  

Individual factors like gender and familiarity can affect the kind of environmental representation that a person acquires during spatial navigation. Men seem to prefer relying on map-like survey representations, while women prefer using sequential route representations. Moreover, a good familiarity with the environment allows more complete environmental representations. This study was aimed at investigating gender differences in two different object-position learning tasks (i.e., Almeria Boxes Tasks) assuming a route or a survey perspective also considering the role of environmental familiarity. Two groups of participants had to learn the position of boxes placed in a virtual room. Participants had several trials, so that familiarity with the environment could increase. In both tasks, the effects of gender and familiarity were found, and only in the route perspective did an interaction effect emerge. This suggests that gender differences can be found regardless of the perspective taken, with men outperforming women in navigational tasks. However, in the route task, gender differences appeared only at the initial phase of learning, when the environment was unexplored, and disappeared when familiarity with the environment increased. This is consistent with studies showing that familiarity can mitigate gender differences in spatial tasks, especially in more complex ones.


Life Sciences ◽  
1995 ◽  
Vol 56 (23-24) ◽  
pp. 2033-2040 ◽  
Author(s):  
J. Romero ◽  
L. Garcia ◽  
M. Cebeira ◽  
D. Zadrozny ◽  
J.J. Fernández-Ruiz ◽  
...  

2019 ◽  
Vol 121 (2) ◽  
pp. 530-548 ◽  
Author(s):  
Rachel C. Yuan ◽  
Sarah W. Bottjer

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird’s own immature song) and the goal motor pattern (each bird’s adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird’s own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.


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