Two separate areas of the brain differentially guide the development of a song control nucleus in the zebra finch.

Akutagawa, Eugene; Konishi, Masakazu

doi:10.1073/pnas.91.26.12413

Cited by 69 publications

(45 citation statements)

References 19 publications

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“…This study shows that ARs and ERs within HVC are necessary for an increase in firing rates and soma area in RA, extending previous, purely morphometric studies of RA afferent input (Herrmann and Arnold, 1991;Akutagawa and Konishi, 1994;Burek et al, 1995;Brenowitz andLent, 2001, 2002). By infusing DHT and E 2 near HVC in SD birds, we demonstrated that coactivation of ARs and ERs in HVC is sufficient for an increase in firing rate and soma area in RA.…”

Section: A Model Of How T and Its Metabolites Induce Changes In Activsupporting

confidence: 87%

Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

Meitzen¹,

Moore²,

Lent³

et al. 2007

J. Neurosci.

102

164

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Steroid sex hormones induce dramatic seasonal changes in reproductive related behaviors and their underlying neural substrates in seasonally breeding vertebrates. For example, in adult white-crowned sparrows, increased Spring photoperiod raises circulating testosterone, causing morphological and electrophysiological changes in song-control nuclei, which modify song behavior for the breeding season. We investigated how photoperiod and steroid hormones induce these changes in morphology, electrophysiology, and behavior. Neurons in a song premotor nucleus, the robust nucleus of the arcopallium (RA), show increased intrinsic spontaneous firing rate and soma size when birds are in breeding condition. Using combinations of systemic and unilateral local intracerebral hormonal manipulations, we show that long-day photoperiod accelerates the effects of systemic testosterone on RA neurons via the estradiol-synthesizing enzyme aromatase (CYP19A1); these changes require inputs from the afferent song control nucleus HVC (used as a proper name) and steroid receptor activation within HVC; local coactivation of androgen and estrogen receptors (ARs and ERs, respectively) within HVC, but not RA, is sufficient to cause neuronal changes in RA; activation of ARs in RA is also permissive. Using bilateral local intracerebral hormone-receptor blockade, we found that ARs and ERs in the song-control nucleus HVC mediate systemic testosterone-induced changes in song stereotypy but not rate. This novel transsynaptic effect of gonadal steroids on activity and morphology of RA neurons is part of a concerted change in key premotor nuclei, enabling stereotyped song.

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Section: A Model Of How T and Its Metabolites Induce Changes In Activsupporting

confidence: 87%

Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

Meitzen¹,

Moore²,

Lent³

et al. 2007

J. Neurosci.

102

164

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“…The absence of topographic organization within the lMAN core 3 RA circuit in juvenile DF/WN birds may affect organization within other circuits as well, such as the projection between the higher vocal center (HVC) and RA that assumes increasing control of song production as vocal learning proceeds (Nottebohm et al, 1982;Akutagawa and Konishi, 1994). Individual RA neurons are contacted by axons from lMAN core as well as from HVC by 20 d in male zebra finches (Mooney and Rao, 1994;Foster and Bottjer, 1998).…”

Section: Discussionmentioning

confidence: 99%

The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches

Iyengar

Bottjer

2002

J. Neurosci.

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The initial establishment of topographic mapping within developing neural circuits is thought to be shaped by innate mechanisms and is primarily independent of experience. Additional refinement within topographic maps leads to precise matching between presynaptic and postsynaptic neurons and is thought to depend on experiential factors during specific sensitive periods in the animal's development. In male zebra finches, axonal projections of the cortical lateral magnocellular nucleus of the anterior neostriatum (lMAN) are critically important for vocal learning. Overall patterns of topographic organization in the majority of these circuits are adult-like throughout the sensitive period for vocal learning and remain stable despite large-scale functional and morphological changes. However, topographic organization within the projection from the core subregion of lMAN (lMAN core ) to the motor cortical robust nucleus of the archistriatum (RA) is lacking at the onset of song development and emerges during the early stages of vocal learning. To study the effects of song-related experience on patterns of axonal connectivity within different song-control circuits, we disrupted song learning by deafening juvenile zebra finches or exposing them to loud white noise throughout the sensitive period for song learning. Depriving juvenile birds of normal auditory experience delayed the emergence of topographic specificity within the lMAN core 3RA circuit relative to age-matched controls, whereas topographic organization within all other projections to and from lMAN was not affected. The projection from lMAN core to RA therefore provides an unusual example of experience-dependent modification of large-scale patterns of brain circuitry, in the sense that auditory deprivation influences the development of overall topographic organization in this pathway.

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“…RA was intensely immunoreactive for TrkB, the receptor for NT-4/5, and it is possible that endogenous auto/paracrine release of NT-4/5 within RA could be regulated by presynaptic input from lMAN (antibodies to recognize NT-4/5 in avian brain are not presently available). With respect to the presence of multiple growth factors in RA, it is important to recognize that RA shows a complex assortment of developmental changes during song learning, including rapid overall growth that is attributable to a substantial increase in the size and spacing of neuronal somata and the delayed arrival of new axons from another cortical song region, HVC (Bottjer et al, 1985(Bottjer et al, , 1986Konishi and Akutagawa, 1985;Nordeen and Nordeen, 1988;Kirn and DeVoogd, 1989;Akutagawa and Konishi, 1994). Because neurotrophins have been shown recently to regulate the growth of somata, dendritic arbors, and axon terminals (Cabelli et al, 1995;Cohen-Cory andFraser, 1995, McAllister et al, 1995;Riddle et al, 1995), it seems likely that multiple anterograde, retrograde, and auto/paracrine signaling pathways could be involved in orchestrating the overall growth and development of RA.…”

Section: Discussionmentioning

confidence: 99%

“…The anatomical basis of redundant trophic signaling may lie in the fact that neuronal populations in the mammalian forebrain generally make and receive a large number of (often reciprocal) synaptic connections with several neuronal populations (Snider, 1994); glial and auto/ paracrine mechanisms of neurotrophin release may also contribute to redundant neurotrophic signaling (Acheson et al, 1995;Yan et al, 1995). By comparison, because the song-control system in the avian forebrain contains large populations of neurons that typically contact a limited number of afferent inputs and efferent targets in a serial, nonreciprocal manner (Bottjer et al, 1989;Johnson et al, 1995;Vates and Nottebohm, 1995), the loss of even one input or target removes a major source of trophic support and can result in extensive anterograde or retrograde neurodegeneration Bottjer, 1993, 1994;Akutagawa and Konishi, 1994). However, even among song-control regions, the requirement for anterograde or retrograde trophic support is transient and appears to wane over the course of juvenile development (e.g., deafferentation of RA ceases to induce neuron death by 40 d of age; Johnson and Bottjer, 1994;cf.…”

Section: Discussionmentioning

confidence: 99%

Neurotrophins Suppress Apoptosis Induced by Deafferentation of an Avian Motor-Cortical Region

et al. 1997

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Studies of the developing nervous system led to the general view that growth factors promote neuronal survival in a "retrograde" manner. For example, release of NGF from postsynaptic peripheral targets followed by uptake and retrograde transport by presynaptic neurons provided a widely accepted conceptual framework for the action of neurotrophins. In contrast, although presynaptic or "anterograde" influences on the survival of developing neurons have been recognized for some time, the mechanisms by which afferent input regulates the survival of postsynaptic cells have received considerably less attention. In the forebrain network for learned vocal behavior in zebra finches, lesions of a cortical region for song control, the lateral magnocellular nucleus of the anterior neostriatum (lMAN), remove presynaptic input to a motor-cortical song region, the robust nucleus of the archistriatum (RA), and cause massive RA neuron death in young birds that are entering the sensitive period for song learning. Here we report that lesions of lMAN followed by infusions of neurotrophins directly into RA completely suppress neuronal apoptosis in RA. Moreover, we show that lMAN neurons are able to transport neurotrophins in the anterograde direction to RA, that neurotrophin-like immunoreactivity is present in cells in lMAN and RA, and that neurotrophin receptor-like immunoreactivity is present in RA. Expression of neurotrophins in lMAN and RA suggests that lMAN presynaptic input could regulate RA neuron survival by synthesizing, transporting, and releasing neurotrophins anterogradely or by regulating the auto/paracrine release of neurotrophins within RA, or perhaps by both. These data provide the first in vivo demonstration that neurotrophins can prevent the death of deafferented cortical neurons, and they raise the possibility that nonretrograde signaling by neurotrophins may be a common means of promoting neuronal survival in the vertebrate telencephalon. Anterograde and auto/ paracrine neurotrophin signaling, along with the more established view that neurotrophins regulate neuron survival via retrograde mechanisms, suggests multidirectional neurotrophin signaling in the vertebrate telencephalon.

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Two separate areas of the brain differentially guide the development of a song control nucleus in the zebra finch.

Cited by 69 publications

References 19 publications

Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

Steroid Hormones Act Transsynaptically within the Forebrain to Regulate Neuronal Phenotype and Song Stereotypy

The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches

Neurotrophins Suppress Apoptosis Induced by Deafferentation of an Avian Motor-Cortical Region

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