Silent Synapses in a Thalamo-Cortical Circuit Necessary for Song Learning in Zebra Finches

2005 ◽  
Vol 94 (6) ◽  
pp. 3698-3707 ◽  
Author(s):  
Sarah W. Bottjer
Keyword(s):  
Failure Rate ◽  
Behavioral Plasticity ◽  
Vocal Learning ◽  
Relative Number ◽  
Song Learning ◽  
Sensitive Period ◽  
Vocal Behavior ◽  
Adult Males ◽  
Silent Synapses

Developmental changes in synaptic properties may act to limit neural and behavioral plasticity associated with sensitive periods. This study characterized synaptic maturation in a glutamatergic thalamo-cortical pathway that is necessary for vocal learning in songbirds. Lesions of the projection from medial dorsolateral nucleus of the thalamus (DLM) to the cortical nucleus lateral magnocellular nucleus of the anterior nidopallium (LMAN) greatly disrupt song behavior in juvenile birds during early stages of vocal learning. However, such lesions lose the ability to disrupt vocal behavior in normal birds at 60–70 days of age, around the time that selective auditory tuning for each bird’s own song (BOS) emerges in LMAN neurons. This pattern has suggested that LMAN is involved in processing song-related information and evaluating the degree to which vocal motor output matches the tutor song to be learned. Analysis of reversed excitatory postsynaptic currents at DLM→LMAN synapses in in vitro slice preparations revealed a pronounced N-methyl-d-aspartate receptor (NMDAR)-mediated component in both juvenile and adult cells with no developmental decrease in the relative contribution of NMDARs to synaptic transmission. However, the synaptic failure rate at DLM→LMAN synapses in juvenile males during the sensitive period for song learning was significantly lower at depolarized potentials than at hyperpolarized potentials. In contrast, the failure rate at DLM→LMAN synapses did not differ at hyper- versus depolarized holding potentials in adult males that had completed the acquisition of a stereotyped song. This pattern indicates that juvenile cells have a higher incidence of silent (NMDAR-only) synapses, which are postsynaptically silent at hyperpolarized potentials due to the voltage-dependent gating of NMDARs. Thus the decreased involvement of the LMAN pathway in vocal behavior is mirrored by a decline in the incidence of silent synapses but not by changes in the relative number of NMDA and AMPA receptors at DLM→LMAN synapses. These findings suggest that a developmental decrease in silent synapses within LMAN may represent a neural correlate of behavioral plasticity during song learning.

scholarly journals Vocal motor changes beyond the sensitive period for song plasticity

2014 ◽  
Vol 112 (9) ◽  
pp. 2040-2052 ◽  
Author(s):  
Logan S. James ◽  
Jon T. Sakata
Keyword(s):  
Behavioral Plasticity ◽  
Sensitive Period ◽  
Vocal Behavior ◽  
Sensorimotor Learning ◽  
Spectral Structure ◽  
Spectral Features ◽  
Change Over Time ◽  
Sensitive Periods ◽  
Over Time ◽  
Support Evidence

Behavior is critically shaped during sensitive periods in development. Birdsong is a learned vocal behavior that undergoes dramatic plasticity during a sensitive period of sensorimotor learning. During this period, juvenile songbirds engage in vocal practice to shape their vocalizations into relatively stereotyped songs. By the time songbirds reach adulthood, their songs are relatively stable and thought to be “crystallized.” Recent studies, however, highlight the potential for adult song plasticity and suggest that adult song could naturally change over time. As such, we investigated the degree to which temporal and spectral features of song changed over time in adult Bengalese finches. We observed that the sequencing and timing of song syllables became more stereotyped over time. Increases in the stereotypy of syllable sequencing were due to the pruning of infrequently produced transitions and, to a lesser extent, increases in the prevalence of frequently produced transitions. Changes in song tempo were driven by decreases in the duration and variability of intersyllable gaps. In contrast to significant changes to temporal song features, we found little evidence that the spectral structure of adult song syllables changed over time. These data highlight differences in the degree to which temporal and spectral features of adult song change over time and support evidence for distinct mechanisms underlying the control of syllable sequencing, timing, and structure. Furthermore, the observed changes to temporal song features are consistent with a Hebbian framework of behavioral plasticity and support the notion that adult song should be considered a form of vocal practice.

scholarly journals Song preferences predict the quality of vocal learning in zebra finches

2021 ◽  
Author(s):  
Carlos A. Rodriguez-Saltos ◽  
Aditya Bhise ◽  
Prasanna Karur ◽  
Ramsha Nabihah Khan ◽  
Sumin Lee ◽  
...  
Keyword(s):  
Reinforcement Schedule ◽  
Social Process ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensitive Period ◽  
Social Reward ◽  
Zebra Finches ◽  
Vocal Development ◽  
Song Preferences

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we hypothesized that the degree to which a juvenile songbird learns a song depends on the degree to which it finds that song rewarding to hear during vocal development. We tested this hypothesis by measuring song preferences in young birds during song learning and then analyzing their adult songs. Song preferences were measured in an operant key-pressing assay. Juvenile male zebra finches (Taeniopygia guttata) had access to two keys, each of which was associated with a higher likelihood of playing the song of their father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a 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 they were themselves singing. At around post-hatch day 60, their preference shifted to the neighbor's song. At the end of the song learning period, we recorded the juveniles' songs and compared them to the father's and the neighbor's song. All of the birds copied 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. Our results show that preference for a social stimulus, in this case a vocalization, predicted social learning during development.

scholarly journals Song in an Affiliative Context Relates to the Neural Expression of Dopamine- and Neurotensin-Related Genes in Male European Starlings

2016 ◽  
Vol 88 (2) ◽  
pp. 81-92 ◽  
Author(s):  
Devin P. Merullo ◽  
Caroline S. Angyal ◽  
Sharon A. Stevenson ◽  
Lauren V. Riters
Keyword(s):  
Vocal Learning ◽  
Song Learning ◽  
Vocal Behavior ◽  
European Starlings ◽  
Dopaminergic Transmission ◽  
D1 And D2 Receptors ◽  
Song Control ◽  
Area X ◽  
Large Groups

Some animals, including songbirds, vocalize at high rates when alone or in large groups. In songbirds, vocal behavior in these contexts is important for song learning and group cohesion. It is not obviously targeted at any particular individual and is described as ‘undirected'. Studies suggest a role for dopamine (DA) in undirected song. The neuropeptide neurotensin (NT) can enhance dopaminergic signaling upon binding to the NT receptor 1 (NTR1) and is found in regions where DA can influence song, including the ventral tegmental area (VTA), septum, and the song control nucleus Area X. To begin to test the hypothesis that NT and DA in these regions interact to influence undirected song, we used quantitative real-time PCR to relate undirected singing to mRNA expression of NT, NTR1, tyrosine hydroxylase (TH; a synthetic enzyme for DA) and D1 and D2 receptors in male European starlings. TH and NT expression in VTA, and NT and D1 expression in Area X, positively correlated with song. NT markers also correlated positively with DA markers in VTA. Given the role of VTA projections to Area X in song learning, these results suggest that interactions between NT and DA in these regions may contribute to vocal learning. In septum, NTR1 expression positively correlated with song and NT and DA markers were correlated, suggesting that NT in this region may influence dopaminergic transmission to facilitate undirected vocalizations. Overall, these findings implicate interactions between NT and DA in affiliative communication.

scholarly journals Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches

2012 ◽  
Vol 107 (4) ◽  
pp. 1142-1156 ◽  
Author(s):  
Vanessa C. Miller-Sims ◽  
Sarah W. Bottjer
Keyword(s):  
Basal Ganglia ◽  
Motor Cortex ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensitive Period ◽  
Cortical Region ◽  
Topographic Organization ◽  
Magnocellular Nucleus ◽  
Auditory Experience ◽  
Dependent Processes

Experience-dependent changes in neural connectivity underlie developmental learning and result in life-long changes in behavior. In songbirds axons from the cortical region LMANcore (core region of lateral magnocellular nucleus of anterior nidopallium) convey the output of a basal ganglia circuit necessary for song learning to vocal motor cortex [robust nucleus of the arcopallium (RA)]. This axonal projection undergoes remodeling during the sensitive period for learning to achieve topographic organization. To examine how auditory experience instructs the development of connectivity in this pathway, we compared the morphology of individual LMANcore→RA axon arbors in normal juvenile songbirds to those raised in white noise. The spatial extent of axon arbors decreased during the first week of vocal learning, even in the absence of normal auditory experience. During the second week of vocal learning axon arbors of normal birds showed a loss of branches and varicosities; in contrast, experience-deprived birds showed no reduction in branches or varicosities and maintained some arbors in the wrong topographic location. Thus both experience-independent and experience-dependent processes are necessary to establish topographic organization in juvenile birds, which may allow birds to modify their vocal output in a directed manner and match their vocalizations to a tutor song. Many LMANcore axons of juvenile birds, but not adults, extended branches into dorsal arcopallium (Ad), a region adjacent to RA that is part of a parallel basal ganglia pathway also necessary for vocal learning. This transient projection provides a point of integration between the two basal ganglia pathways, suggesting that these branches convey corollary discharge signals as birds are actively engaged in learning.

scholarly journals Open-ended song learning in a hummingbird

2013 ◽  
Vol 9 (5) ◽  
pp. 20130625 ◽  
Author(s):  
Marcelo Araya-Salas ◽  
Timothy Wright
Keyword(s):  
Vocal Learning ◽  
Early Learning ◽  
Song Learning ◽  
Sensitive Period ◽  
First Year ◽  
Song Type ◽  
Song Repertoire ◽  
First Year Of Life ◽  
Song Types ◽  
Avian Group

Vocal learning in birds is typically restricted to a sensitive period early in life, with the few exceptions reported in songbirds and parrots. Here, we present evidence of open-ended vocal learning in a hummingbird, the third avian group with vocal learning. We studied vocalizations at four leks of the long-billed hermit Phaethornis longirostris during a four-year period. Individuals produce a single song repertoire, although several song-types can coexist at a single lek. We found that nine of 49 birds recorded on multiple days (18%) changed their song-type between consecutive recordings. Three of these birds replaced song-types twice. Moreover, the earliest estimated age when song replacement occurred ranged from 186 to 547 days (mean = 307 days) and all nine birds who replaced song-types produced a crystallized song before replacement. The findings indicate that song-type replacement is distinct from an initial early learning sensitive period. As half of lekking males do not survive past the first year of life in this species, song learning may well extend throughout the lifespan. This behaviour would be convergent to vocal learning programmes found in parrots and songbirds.

Birdsong learning in the laboratory, with especial reference to the song of the Zebra Finch (Taeniopygia guttata)

2011 ◽  
Vol 12 (2) ◽  
pp. 324-350 ◽  
Author(s):  
Sébastien Derégnaucourt
Keyword(s):  
Zebra Finch ◽  
Social Influences ◽  
Vocal Learning ◽  
Taeniopygia Guttata ◽  
Speech Development ◽  
Song Learning ◽  
Sensitive Period ◽  
Experimental Conditions ◽  
Young Bird ◽  
Advantages And Disadvantages

Vocal imitation in songbirds exhibits interesting parallels to infant speech development and is currently the model system of choice for exploring the behavioural, molecular and electrophysiological substrates of vocal learning. Among songbirds, the Zebra Finch (Taeniopygia guttata) is currently used as the ‘flying mouse’ of birdsong research. Only males sing and they develop their song primarily during a short sensitive period in early life. They learn their speciesspecific song patterns by memorizing and imitating the songs of conspecifics, mainly adults. Since Immelmann's pioneering work, thousands of zebra finches have been raised in strictly controlled auditory environments to examine how their experience affected their songs. In this article, I review the different experimental procedures that have been used in the laboratory to study the social influences on song learning in the Zebra Finch. Poor song learning was observed using passive playback of taped songs, whereas self-eliciting exposure using operant tutoring techniques induced significant learning, but with a high interindividual variability. The success of the training paradigm is often measured by the quality of imitation of the songs to which the young bird is exposed. Using empirical evidence from the field and the laboratory, I will also discuss this issue, by summarizing possible advantages and disadvantages of producing a perfect imitation. So far, the best method to get a close copy of a song model in the Zebra Finch is to place a single young bird with an adult male. This situation, which is rather unnatural, does not meet the criteria for precise control necessary in experimental conditions. Optimizing the methods used to train a zebra finch to learn a song, in order to be able to predict the imitation success, will improve our understanding of the dynamics of vocal production learning. It would also consolidate this species as a research model of relevance to human speech development and disorders. Keywords: Zebra Finch; birdsong; learning; development; memory; social influences

scholarly journals Good tutors are not Dear Enemies in Song Sparrows

2017 ◽  
Author(s):  
Çağlar Akçay ◽  
S. Elizabeth Campbell ◽  
Michael D. Beecher
Keyword(s):  
Learning Strategies ◽  
Social Factors ◽  
Vocal Learning ◽  
Song Learning ◽  
Adult Males ◽  
Young Males ◽  
Song Sparrows ◽  
Field Evidence ◽  
High Aggression ◽  
Cooperative Relationship

AbstractBird song is the most widely studied example of vocal learning outside human language and shares important parallels with it, including the importance of social factors during development. Our understanding of how social factors affect song learning however remains surprisingly incomplete. Here we examine the possible role of aggressive interactions in determining song “tutor” choice in song sparrows (Melospiza melodia), a songbird in which individuals display song learning strategies ranging from learning primarily from one tutor, to learning a few songs each from a number of tutors. We test two hypotheses: The Competition hypothesis suggests that young birds learn more from tutors with whom they compete especially intensely and predicts that tutees will respond with high aggression to tutor songs. In contrast the Cooperation hypothesis suggests that song learning reflects a cooperative relationship between the tutor and the tutee and predicts that tutees will respond with low aggression to tutor songs. In a playback experiment we found that birds respond more aggressively to songs of their tutors than they do to songs of strangers and that the strength of aggressive response correlated positively with how much they had learned from that tutor. These results provide the first field evidence for the hypothesis that young males preferentially learn their songs from adult males with whom they compete most intensely during the song-learning phase, and perhaps afterwards.

scholarly journals Adding colour-realistic video images to audio playbacks increases stimulus engagement but does not enhance vocal learning in zebra finches

2021 ◽  
Author(s):  
Judith M. Varkevisser ◽  
Ralph Simon ◽  
Ezequiel Mendoza ◽  
Martin How ◽  
Idse van Hijlkema ◽  
...  
Keyword(s):  
Visual Cues ◽  
Sound Production ◽  
Visual Stimuli ◽  
Vocal Learning ◽  
Song Learning ◽  
Frame Rate ◽  
Zebra Finches ◽  
Video Content ◽  
Biologically Relevant ◽  
Video Images

AbstractBird song and human speech are learned early in life and for both cases engagement with live social tutors generally leads to better learning outcomes than passive audio-only exposure. Real-world tutor–tutee relations are normally not uni- but multimodal and observations suggest that visual cues related to sound production might enhance vocal learning. We tested this hypothesis by pairing appropriate, colour-realistic, high frame-rate videos of a singing adult male zebra finch tutor with song playbacks and presenting these stimuli to juvenile zebra finches (Taeniopygia guttata). Juveniles exposed to song playbacks combined with video presentation of a singing bird approached the stimulus more often and spent more time close to it than juveniles exposed to audio playback only or audio playback combined with pixelated and time-reversed videos. However, higher engagement with the realistic audio–visual stimuli was not predictive of better song learning. Thus, although multimodality increased stimulus engagement and biologically relevant video content was more salient than colour and movement equivalent videos, the higher engagement with the realistic audio–visual stimuli did not lead to enhanced vocal learning. Whether the lack of three-dimensionality of a video tutor and/or the lack of meaningful social interaction make them less suitable for facilitating song learning than audio–visual exposure to a live tutor remains to be tested.

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