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.

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 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 Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

2019 ◽  
Author(s):  
Daniel M. Vahaba ◽  
Amelia Hecsh ◽  
Luke Remage-Healey
Keyword(s):  
Memory Consolidation ◽  
Temporal Cortex ◽  
Vocal Learning ◽  
Song Learning ◽  
Auditory Memory ◽  
Vocal Imitation ◽  
Neural Representations ◽  
Estrogen Synthesis ◽  
Auditory Experience ◽  
Caudomedial Nidopallium

ABSTRACTBirdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are formed and consolidated. In both adults and developing songbirds, there is strong evidence suggesting the caudomedial nidopallium (NCM), a higher order auditory forebrain area, is the site of auditory memory consolidation. However, the mechanisms that facilitate this consolidation are poorly understood. One likely mechanism is 17β-estradiol (E2), which is associated with speech-language development and disorders in humans, and is abundant in both mammalian temporal cortex and songbird NCM. Circulating E2 is also elevated during the auditory memory phase, and in NCM immediately after song learning sessions, suggesting it functions to encode recent auditory experience. Therefore, we tested a role for E2 production in auditory memory consolidation during development using a comprehensive set of investigations to ask this question at the level of neuroanatomy, neurophysiology, and behavior. Our results demonstrate that while systemic estrogen synthesis blockade regulates juvenile song production, inhibiting E2 synthesis locally within NCM does not adversely affect song learning outcomes. Surprisingly, early life E2 manipulations in NCM modify the neural representations of birds’ own song and the model tutor song in both NCM and a downstream sensorimotor nucleus (HVC). Further, we show that the capacity to synthesize neuroestrogens remains high throughout development alongside substantial changes in NCM cell density across age. Taken together, these findings suggest that E2 plays a multifaceted role during development, and demonstrate that contrary to prediction, unilateral post-training estrogen synthesis blockade in the auditory cortex does not negatively impact vocal learning. Acute downregulation of neuroestrogens are therefore likely permissive for juvenile auditory memorization, while neuroestrogen synthesis influences communication production and representation in adulthood.

scholarly journals Conjunction of Vocal Production and Perception Regulates Expression of the Immediate Early Gene ZENK in a Novel Cortical Region of Songbirds

2010 ◽  
Vol 103 (4) ◽  
pp. 1833-1842 ◽  
Author(s):  
Sarah W. Bottjer ◽  
Tanya L. Alderete ◽  
Daniel Chang
Keyword(s):  
Vocal Learning ◽  
Early Gene ◽  
Vocal Behavior ◽  
Projection Neurons ◽  
Cortical Region ◽  
Developmentally Regulated ◽  
Vocal Production ◽  
Cortical Nucleus ◽  
Magnocellular Nucleus ◽  
Low Levels

The cortical nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium) provides the output of a basal ganglia pathway that is necessary for acquisition of learned vocal behavior during development in songbirds. LMAN is composed of two subregions, a core and a surrounding shell, that give rise to independent pathways that traverse the forebrain in parallel. The LMANshell pathway forms a recurrent loop that includes a cortical region, the dorsal region of the caudolateral nidopallium (dNCL), hitherto unknown to be involved with learned vocal behavior. Here we show that vocal production strongly induces the IEG product ZENK in dNCL of zebra finches. Hearing tutor song while singing is more effective at inducing expression in dNCL of juvenile birds during the auditory–motor integration stage of vocal learning than is hearing conspecific song. In contrast, hearing conspecific song is relatively more effective at inducing expression in adult birds, regardless of whether they are producing song. Furthermore, ZENK+ neurons in dNCL include projection neurons that are part of the LMANshell recurrent loop and a high proportion of dNCL projection neurons express ZENK in singing juvenile birds that hear tutor song. Thus juvenile birds that are actively refining their vocal pattern to imitate a tutor song show high levels of ZENK induction in dNCL neurons when they are singing while hearing the song of their tutor and low levels when they hear a novel conspecific. This pattern indicates that dNCL is a novel brain region involved with vocal learning and that its function is developmentally regulated.

scholarly journals A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

2017 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Leblanc ◽  
Arthur Leblois
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensorimotor Learning ◽  
Zebra Finches ◽  
Subcortical Structures ◽  
Song Production ◽  
Cerebellar Lesions ◽  
Avian Song

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.

Imaging Brain Metabolism in the Newborn

2018 ◽  
Vol 33 (13) ◽  
pp. 851-860 ◽  
Author(s):  
Harry T. Chugani
Keyword(s):  
Basal Ganglia ◽  
Motor Cortex ◽  
Brain Stem ◽  
Spatial Resolution ◽  
Neonatal Intensive Care ◽  
Glucose Utilization ◽  
High Spatial Resolution ◽  
Sensitive Period ◽  
Temporal Region ◽  
Positron Emission

In this review, we discuss molecular brain imaging studies using positron emission tomography (PET) with 2-deoxy-2(18F)fluoro-d-glucose (FDG) in human newborns and infants, and illustrate how this technology can be applied to probe the neuropathophysiology of neonatal neurologic disorders. PET studies have been difficult to perform in sick babies because of patient transportation issues and suboptimal spatial resolution. With approval from the FDA and the institutional review board, we modified and installed the Focus 220 animal microPET scanner (Concorde Microsystems, Knoxville, TN) directly in our neonatal intensive care unit in Children’s Hospital of Michigan and verified the high spatial resolution (<2 mm full-width-at-half-maximum) of this microPET. The neonatal pattern of glucose metabolism is very consistent, with the highest degree of activity in primary sensory and motor cortex, medial temporal region, thalamus, brain stem, and cerebellar vermis. Prior studies have shown that increases of glucose utilization are seen by 2 to 3 months in the parietal, temporal, cingulate, and primary visual cortex; basal ganglia; and cerebellar hemispheres. Between 6 and 8 months, lateral and inferior frontal cortex becomes more functionally active and, eventually, between 8 and 12 months, the dorsal and medial frontal regions also show a maturational increase. These findings are consistent with the physical, behavioral, and cognitive maturation of the infant. At birth, metabolic rates of glucose utilization in cortex are about 30% lower than in adults but rapidly rise such that, by 3 years, the cerebral cortical rates exceed adult rates by more than 2-fold. At around puberty, the rates for cerebral cortex begin to decline and gradually reach adult values by 16-18 years. These nonlinear changes of glucose utilization indirectly reflect programed periods of synaptic proliferation and pruning in the brain. Positron emission tomographic (PET) imaging of GABAA receptors (using 11C-flumazenil) in newborns also show a pattern very different from adults, with high binding in amygdala-hippocampus, sensory-motor cortex, thalamus, brain stem, and basal ganglia, in that order. We speculate that the early development of amygdala/hippocampus prepares the baby for bonding, attachment, and memory, and the deprivation of such experiences during a sensitive period results in malfunction of these networks and psychopathology, as has been shown in studies on severely socioemotionally deprived children. Recently developed hybrid PET/magnetic resonance (MR) scanners allow the simultaneous acquisition of PET and MR data sets with advanced applications. These devices are particularly advantageous for scanning babies and infants because of the high spatial resolution, automated coregistration of anatomical and functional images and, in the case of need for sedation, maximal data acquired in 1 session.

Sleep-Related Neural Activity in a Premotor and a Basal-Ganglia Pathway of the Songbird

2006 ◽  
Vol 96 (2) ◽  
pp. 794-812 ◽  
Author(s):  
Richard H. R. Hahnloser ◽  
Alexay A. Kozhevnikov ◽  
Michale S. Fee
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Spike Trains ◽  
Projection Neurons ◽  
Time Lags ◽  
Reversible Inactivation ◽  
Magnocellular Nucleus ◽  
Area X ◽  
Temporal Sequences ◽  
Spike Patterns

During singing, neurons in premotor nucleus RA (robust nucleus of the arcopallium) of the zebra finch produce complex temporal sequences of bursts that are recapitulated during sleep. RA receives input from nucleus HVC via the premotor pathway, and also from the lateral magnocellular nucleus of the anterior nidopallium (LMAN), part of a basal ganglia-related circuit essential for vocal learning. We explore the propagation of sleep-related spike patterns in these two pathways and their influences on RA activity. We promote sleep in head-fixed birds by injections of melatonin and make single-neuron recordings from the three major classes of neurons in HVC: RA-projecting neurons, Area X-projecting neurons, and interneurons. We also record LMAN neurons that project to RA. In paired recordings, spike trains from identified HVC neuron types are strongly coherent with spike trains in RA neurons, whereas LMAN projection neurons on average exhibit only a weak coherency with neurons in HVC and RA. We further examine the relative roles of HVC and LMAN in generating RA burst sequences with reversible inactivation. Lidocaine inactivation of HVC completely abolishes bursting in RA, whereas inactivation of LMAN has no effect on burst rates in RA. In combination, our data suggest that in adult birds, RA burst sequences in sleep are driven via the premotor pathway from HVC. We present a simple generative model of spike trains in HVC, RA, and LMAN neurons that is able to qualitatively reproduce observed coherency functions. We propose that commonly observed coherency peaks at positive and negative time lags are caused by sequentially correlated HVC activity.

scholarly journals A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Le Blanc ◽  
Carole Levenes ◽  
Arthur Leblois
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensorimotor Learning ◽  
Zebra Finches ◽  
Subcortical Structures ◽  
Song Production ◽  
Cerebellar Lesions ◽  
Avian Song

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.

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.

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