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Eliot A. Brenowitz - One of the best experts on this subject based on the ideXlab platform.
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Neurogenesis in the Adult Avian Song-Control System
Cold Spring Harbor perspectives in biology, 2015Co-Authors: Eliot A. Brenowitz, Tracy A. LarsonAbstract:New neurons are added throughout the forebrain of adult birds. The song-control system is a model to investigate the addition of new long-projection neurons to a cortical circuit that regulates song, a learned sensorimotor behavior. Neuroblasts destined for the song nucleus HVC arise in the walls of the lateral ventricle, and wander through the pallium to reach HVC. The survival of new HVC neurons is supported by gonadally secreted testosterone and its downstream effectors including neurotrophins, vascularization, and electrical activity of postsynaptic neurons in nucleus RA (robust nucleus of the Arcopallium). In seasonal species, the HVC→RA circuit degenerates in nonbreeding birds, and is reconstructed by the incorporation of new projection neurons in breeding birds. There is a functional linkage between the death of mature HVC neurons and the birth of new neurons. Various hypotheses for the function of adult neurogenesis in the song system can be proposed, but this remains an open question.
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Postsynaptic neural activity regulates neuronal addition in the adult avian song control system
Proceedings of the National Academy of Sciences of the United States of America, 2013Co-Authors: Tracy A. Larson, Tsu Wei Wang, Samuel D. Gale, Kimberly E. Miller, Nivretta M. Thatra, Melissa L. Caras, David J. Perkel, Eliot A. BrenowitzAbstract:A striking feature of the nervous system is that it shows extensive plasticity of structure and function that allows animals to adjust to changes in their environment. Neural activity plays a key role in mediating experience-dependent neural plasticity and, thus, creates a link between the external environment, the nervous system, and behavior. One dramatic example of neural plasticity is ongoing neurogenesis in the adult brain. The role of neural activity in modulating neuronal addition, however, has not been well studied at the level of neural circuits. The avian song control system allows us to investigate how activity influences neuronal addition to a neural circuit that regulates song, a learned sensorimotor social behavior. In adult white-crowned sparrows, new neurons are added continually to the song nucleus HVC (proper name) and project their axons to its target nucleus, the robust nucleus of the Arcopallium (RA). We report here that electrical activity in RA regulates neuronal addition to HVC. Decreasing neural activity in RA by intracerebral infusion of the GABAA receptor agonist muscimol decreased the number of new HVC neurons by 56%. Our results suggest that postsynaptic electrical activity influences the addition of new neurons into a functional neural circuit in adult birds.
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Testosterone and brain-derived neurotrophic factor interactions in the avian song control system
Neuroscience, 2012Co-Authors: Eliot A. BrenowitzAbstract:Interaction between steroid sex hormones and brain-derived neurotrophic factor (BDNF) is a common feature of vertebrate brain organization. The avian song control system provides an excellent model for studying such interactions in neural circuits that regulate song, a learned sensorimotor behavior that is often sexually dimorphic and restricted to reproductive contexts. Testosterone (T) and its steroid metabolites interact with BDNF during development of the song system and in adult plasticity, including the addition of newborn neurons to the pallial nucleus HVC and seasonal changes in structure and function of these circuits. T and BDNF interact locally within HVC to influence cell proliferation and survival. This interaction may also occur transsynpatically; T increases the synthesis of BDNF in HVC, and BDNF protein is then released on to postsynaptic cells in the robust nucleus of the Arcopallium (RA) where it has trophic effects. The interaction between sex steroids and BDNF is an example of molecular exploitation, with the evolutionarily ancient steroid-receptor complex having been captured by the more recently evolved BDNF. The functional linkage of sex steroids to BDNF may be of adaptive value in regulating the trophic effects of the neurotrophin in sexually dimorphic and reproductively relevant contexts.
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Seasonal changes in androgen receptor mRNA in the brain of the white-crowned sparrow.
General and comparative endocrinology, 2009Co-Authors: Gregory S. Fraley, Karin Lent, Robert A. Steiner, Eliot A. BrenowitzAbstract:In songbirds, neurons that regulate learned song behavior undergo extensive seasonal plasticity in their number and size in relation to the bird's reproductive status. Seasonal plasticity of these brain regions is primarily regulated by changes in circulating concentrations of testosterone. Androgen receptors are present in all of the major song nuclei, but it is unknown whether levels of androgen receptor mRNA in the telencephalic song regions HVC, the robust nucleus of the Arcopallium, and the lateral magnocellular nucleus of the anterior nidopallium change as a function of season in white-crowned sparrows. To determine whether seasonal changes in levels of androgen receptor mRNA are specific to the song control system, we also measured levels of androgen receptor mRNA in a limbic nucleus, the lateral division of the bed nucleus of the stria terminalis (the lateral division of the bed nucleus of the stria terminalis). We found that levels of androgen receptor mRNA were higher in HVC and the lateral division of the bed nucleus of the stria terminalis of birds in the breeding condition compared with the nonbreeding condition; however, we observed no seasonal differences in levels of androgen receptor mRNA in either the robust nucleus of the Arcopallium or the lateral magnocellular nucleus of the anterior nidopallium. These results are consistent with previous observations that seasonal plasticity of the song nuclei results from testosterone acting directly on HVC, which then exerts transsynaptic trophic effects on its efferent targets. The seasonal change in the expression of androgen receptor in HVC may be one component of the cellular mechanisms underlying androgenic effects on seasonal plasticity of the song control nuclei.
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The Role of Neurotrophins in the Seasonal-Like Growth of the Avian Song Control System
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2009Co-Authors: Anne Marie Wissman, Eliot A. BrenowitzAbstract:The avian song control system undergoes pronounced seasonal plasticity in response to photoperiod and hormonal cues. The action of testosterone (T) and its metabolites in the song nucleus HVC is both necessary and sufficient to promote breeding season-like growth of its efferent nuclei RA (robust nucleus of the Arcopallium) and Area X, suggesting that HVC may release a trophic factor such as brain-derived neurotrophic factor (BDNF) into RA and X. BDNF is involved in many forms of adult neural plasticity in other systems and is present in the avian song system. We used a combination of in situ hybridization and intracerebral infusions to test whether BDNF plays a role in the seasonal-like growth of the song system in adult male white-crowned sparrows. BDNF mRNA levels increased in HVC in response to breeding conditions, and BDNF infusion into RA was sufficient to promote breeding-like changes in somatic area and neuronal density. Expression of the mRNA for the Trk B receptor of BDNF, however, did not vary with seasonal conditions in either HVC or RA. Local blockade of BDNF activity in RA via infusion of Trk-Fc fusion proteins inhibited the response to breeding conditions. Our results indicate that BDNF is sufficient to promote the seasonal plasticity in somatic area and cell density in RA, although NT-3 may also contribute to this process, and suggest that HVC may be a presynaptic source of increased levels of BDNF in RA of breeding-condition birds.
Lauren V. Riters - One of the best experts on this subject based on the ideXlab platform.
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neurotensin and neurotensin receptor 1 mrna expression in song control regions changes during development in male zebra finches
Developmental Neurobiology, 2018Co-Authors: Devin P Merullo, Chinweike Norman Asogwa, Miguel Sanchezvalpuesta, Shin Hayase, Bikash R Pattnaik, Kazuhiro Wada, Lauren V. RitersAbstract:Learned vocalizations are important for communication in some vertebrate taxa. The neural circuitry for the learning and production of vocalizations is well known in songbirds, many of which learn songs initially during a critical period early in life. Dopamine is essential for motor learning, including song learning, and dopamine-related measures change throughout development in song-control regions such as HVC, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), Area X, and the robust nucleus of the Arcopallium (RA). In mammals, the neuropeptide neurotensin strongly interacts with dopamine signaling. This study investigated a potential role for the neurotensin system in song learning by examining how neurotensin (Nts) and neurotensin receptor 1 (Ntsr1) expression change throughout development. Nts and Ntsr1 mRNA expression was analyzed in song-control regions of male zebra finches in four stages of the song learning process: pre-subsong (25 days posthatch; dph), subsong (45 dph), plastic song (60 dph), and crystallized song (130 dph). Nts expression in LMAN during the subsong stage was lower compared to other time points. Ntsr1 expression was highest in HVC, Area X, and RA during the pre-subsong stage. Opposite and complementary expression patterns for the two genes in song nuclei and across the whole brain suggest distinct roles for regions that produce and receive Nts. The expression changes at crucial time points for song development are similar to changes observed in dopamine studies and suggest Nts may be involved in the process of vocal learning. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 671-686, 2018.
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Patterns of FOS protein induction in singing female starlings
Behavioural brain research, 2012Co-Authors: Jesse M.s. Ellis, Lauren V. RitersAbstract:Females of many songbird species produce song, but information about the neural correlates of singing behavior is limited in this sex. Although well studied in males, activity in premotor song control regions and social behavior regions has not been examined in females during song production. Here, we examined the immediate early gene protein product FOS in both song control and social behavior brain regions after female starlings defending nest boxes responded to an unfamiliar female in a naturalistic setting. We found that females that sang in response to the intruder had much higher numbers of fos-immunoreactive neurons (fos-ir) in the vocal control regions HVC, the robust nucleus of the Arcopallium (RA), and the dorsomedial part of the nucleus intercollicularis (DM of the ICo). In HVC, fos-ir correlated positively with song length. In RA, DM and Area X, fos-ir correlated positively with number of songs produced. In social behavior regions, singers showed higher fos-ir in the nucleus taeniae of the amygdala, the dorsal part of the bed nucleus of the stria terminalis, and the ventromedial hypothalamus than non-singers. Overall, patterns of fos-ir in song control regions in females were similar to those reported for males, but differences in fos-ir were identified in social behavior regions. These differences may reflect a distinct role for brain regions involved in social behavior in female song, or they may reflect differences in the social function of female and male song.
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Seasonal Plasticity in the Song Control System: Multiple Brain Sites of Steroid Hormone Action and the Importance of Variation in Song Behavior
Annals of the New York Academy of Sciences, 2004Co-Authors: Gregory F Ball, Lauren V. Riters, Catherine J. Auger, Daniel J. Bernard, Thierry Charlier, Jennifer J. Sartor, Jacques BalthazartAbstract:Birdsong, in non-tropical species, is generally more common in spring and summer when males sing to attract mates and/or defend territories. Changes in the volumes of song control nuclei, such as HVC and the robust nucleus of the Arcopallium (RA), are observed seasonally. Long photoperiods in spring stimulate the recrudescence of the testes and the release of testosterone. Androgen receptors, and at times estrogen receptors, are present in HVC and RA as are co-factors that facilitate the transcriptional activity of these receptors. Thus testosterone can act directly to induce changes in nucleus volume. However, dissociations have been identified at times among long photoperiods, maximal concentrations of testosterone, large song control nuclei, and high rates of song. One explanation of these dissociations is that song behavior itself can influence neural plasticity in the song system. Testosterone can act via brain-derived neurotrophic factor (BDNF) that is also released in HVC as a result of song activity. Testosterone could enhance song nucleus volume indirectly by acting in the preoptic area, a region regulating sexual behaviors, including song, that connects to the song system through catecholaminergic cells. Seasonal neuroplasticity in the song system involves an interplay among seasonal state, testosterone action, and behavioral activity.
Monika Sadananda - One of the best experts on this subject based on the ideXlab platform.
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Afferentation of a caudal forebrain area activated during courtship behavior: a tracing study in the zebra finch (Taeniopygia guttata).
Brain research, 2007Co-Authors: Monika Sadananda, Stefan Korte, Hans-joachim BischofAbstract:A caudal forebrain area of zebra finches that comprises a part of the caudal nidopallium and a part of the intermediate Arcopallium is highly activated during courtship. This activation is thought to reflect the processing of information that is necessary for the choice of an appropriate mate. In addition to the information on the potential mate, control of courtship behavior includes motivational aspects. Being involved in the integration of external input and previously stored information, as well as in adding motivational factors, the caudal nidopallium and intermediate Arcopallium should be integrative areas receiving input from many other regions of the brain. Our results indeed show that the caudal nidopallium receives input from a variety of telencephalic regions including the secondary visual and auditory areas. The intermediate Arcopallium is recipient of input from intermediate and caudal nidopallium, mesopallium and densocellular hyperpallium. Regions closely associated with the song control nuclei also innervate both regions. There are also specific visual and auditory thalamic inputs, while specific motivating catecholaminergic mesencephalic afferents include the ventral tegmental area, the substantia nigra and the locus coeruleus. In addition, non-specific activation reaches these areas from the mesencephalic reticular formation. Bilateral innervation by ventral intermediate Arcopallium indicates links with sensori-motor pathways, while the projection from the caudal nidopallium to intermediate Arcopallium suggests monosynaptic and disynaptic input to downstream motor pathways. These findings support the idea of an involvement of the caudal nidopallium and the intermediate Arcopallium in the control of courtship behavior.
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Afferentation of the lateral nidopallium: A tracing study of a brain area involved in sexual imprinting in the zebra finch (Taeniopygia guttata).
Brain research, 2006Co-Authors: Monika Sadananda, Hans-joachim BischofAbstract:The lateral forebrain of zebra finches that comprises parts of the lateral nidopallium and parts of the lateral mesopallium is supposed to be involved in the storage and processing of visual information acquired by an early learning process called sexual imprinting. This information is later used to select an appropriate sexual partner for courtship behavior. Being involved in such a complicated behavioral task, the lateral nidopallium should be an integrative area receiving input from many other regions of the brain. Our experiments indeed show that the lateral nidopallium receives input from a variety of telencephalic regions including the primary and secondary areas of both visual pathways, the globus pallidus, the caudolateral nidopallium functionally comparable to the prefrontal cortex, the caudomedial nidopallium involved in song perception and storage of song-related memories, and some parts of the Arcopallium. There are also a number of thalamic, mesencephalic, and brainstem efferents including the catecholaminergic locus coeruleus and the unspecific activating reticular formation. The spatial distribution of afferents suggests a compartmentalization of the lateral nidopallium into several subdivisions. Based on its connections, the lateral nidopallium should be considered as an area of higher order processing of visual information coming from the tectofugal and the thalamofugal visual pathways. Other sensory modalities and also motivational factors from a variety of brain areas are also integrated here. These findings support the idea of an involvement of the lateral nidopallium in imprinting and the control of courtship behavior.
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Acetylcholinesterase in central vocal control nuclei of the zebra finch (Taeniopygia guttata)
Journal of Biosciences, 2004Co-Authors: Monika SadanandaAbstract:The distribution of acetylcholinesterase (AChE) in the central vocal control nuclei of the zebra finch was studied using enzyme histochemistry. AChE fibres and cells are intensely labelled in the forebrain nucleus area X, strongly labelled in high vocal centre (HVC) perikarya, and moderately to lightly labelled in the somata and neuropil of vocal control nuclei robust nucleus of Arcopallium (RA), medial magnocellular nucleus of the anterior nidopallium (MMAN) and lateral magnocellular nucleus of the anterior nidopallium (LMAN). The identified sites of cholinergic and/or cholinoceptive neurons are similar to the cholinergic presence in vocal control regions of other songbirds such as the song sparrow, starling and another genus of the zebra finch ( Poephila guttata ), and to a certain extent in parallel vocal control regions in vocalizing birds such as the budgerigar. AChE presence in the vocal control system suggests innervation by either afferent projecting cholinergic systems and/or local circuit cholinergic neurons. Co-occurrence with choline acetyltransferase (ChAT) indicates efferent cholinergic projections. The cholinergic presence in parts of the zebra finch vocal control system, such as the area X, that is also intricately wired with parts of the basal ganglia, the descending fibre tracts and brain stem nuclei could underlie this circuitry’s involvement in sensory processing and motor control of song.
András Csillag - One of the best experts on this subject based on the ideXlab platform.
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Multiple amygdaloid divisions of Arcopallium send convergent projections to the nucleus accumbens and neighboring subpallial amygdala regions in the domestic chicken: a selective pathway tracing and reconstruction study
Brain Structure and Function, 2017Co-Authors: János Hanics, Gyöngyi Teleki, Alán Alpár, Andrea D. Székely, András CsillagAbstract:Retrograde tracing with choleratoxin B, injected into the nucleus accumbens (Ac) and bed nucleus of stria terminalis, lateral part (BSTL), yielded labeled perikarya in a ring-shaped area of Arcopallium, including dorsal and hilar subdivisions, with a wedge-shaped node of dense accumulation in the amygdalopiriform area (APir). Also, the position of source neurons for this arcopallio-subpallial pathway was verified by anterograde tracing. Three subregions of Arcopallium (amygdalopiriform, dorsal, hilar) were injected with dextran (10 kDa), and fibers and terminal fields were detected in Ac, BSTL and extended amygdala (EA). Most abundant projections to Ac arose from APir. The study enabled precise description of the main output fiber streams: the dorsal stream follows the dorsal border of Arcopallium and, continuing in the ventral amygdalofugal tract, it traverses the EA and the BSTL before reaching the Ac. The ventral stream of fibers enters the EA along the ventral subpallial border and terminates in the basal nucleus and ventral pallidum. The course of the pathway was reconstructed in 3D. Retrogradely labeled arcopallial neurons were devoid of DARPP-32. DARPP-32 was present in the Ac but not the BSTL. No colocalization between the calcium binding proteins calbindin, parvalbumin and calretinin, and retrogradely labeled neurons was detected, despite a considerable territorial overlap. This finding further supports the excitatory nature of the arcopallial-accumbens pathway. Conjoint and convergent amygdalar input to EA, including BSTL, as well as to Ac subregions likely transmits fear and aggression related signals to both viscerolimbic (EA) and learned reward- and motivation-related (Ac) ventrobasal forebrain regions.
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Distribution of vasotocin- and vasoactive intestinal peptide-like immunoreactivity in the brain of penduline tit
European journal of anatomy, 2016Co-Authors: Catherine M. Montagnese, Tamás Székely, András Csillag, Gergely ZacharAbstract:Penduline tits are songbirds, used as model animals in numerous studies of sexual conflict. Nevertheless, the distribution of neuropeptides in the brain of this avian species remains largely unknown. Here we present some of the first results on distribution of vasotocin (AVT) and vasoactive intestinal peptide (VIP) in the brain of this songbird species, using immunohistochemical mapping. The bulk of AVT-like cells are found in the hypothalamic supraoptic, paraventricular and suprachiasmatic nuclei, medial bed nucleus of the stria terminalis, and along the lateral forebrain bundle. Most AVT-like fibres course toward the median eminence, but also in the medial bed nucleus of the stria terminalis, preoptic area and lateral septum. Further terminal fields occur in the dorsal thalamus, ventral tegmental area and pretectal area. Most VIP-like cells are in the lateral septal organ and arcuate nucleus. VIP-like fibres are distributed extensively in the hypothalamus, preoptic area, lateral septum, nucleus of the diagonal band. They are also found in the medial bed nucleus of the stria terminalis, amygdaloid nucleus of taenia, robust nucleus of the Arcopallium, caudo-ventral hyperpallium, nucleus accumbens and the brainstem. The results indicate a high degree of conservatism in both AVT and VIP neuropeptidergic systems across avian species, as well as the different vertebrate taxa. The anatomical distribution of AVT and VIP in the penduline tit supports an involvement of these peptides in reproductive behaviours and social decision making, widely studied in this wild bird species.
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localized lesions of Arcopallium intermedium of the lateral forebrain caused a handling cost aversion in the domestic chick performing a binary choice task
European Journal of Neuroscience, 2006Co-Authors: Naoya Aoki, András Csillag, Toshiya MatsushimaAbstract:Behavioral effects of handling cost (time and/or energetic cost for food consumption) on choice were examined using domestic chicks trained in operant task reinforced by delayed food rewards. When scattered sesame was delivered in more demanding conditions, a colored cue bead associated with six grains ('large' and 'costly' reward) was chosen progressively less frequently against another bead associated with one grain ('small' and 'not costly' reward). The choice thus proved to be highly sensitive to the anticipated handling cost. Excitotoxic lesion of the bilateral Arcopallium intermedium also selectively reduced the choice of the six grains, while leaving actual cost investment (number of pecks and handling time) unaltered. No significant changes occurred in choices between one grain of sesame ('small' and 'not costly' reward) and one grain of barley (or a ball composed of six sesame grains glued by starch; 'large' and 'not costly' reward), indicating that choice based on anticipated food amount was not impaired. On the other hand, lesion of the ventral striatum did not change the choice ratio in any trial types. Operant peck latencies somewhat depended on food rewards, but were not affected by lesions of the Arcopallium or the ventral striatum. The Arcopallium could contribute to foraging behaviors by enabling chicks to overcome the handling cost, thus gaining more beneficial food. Furthermore, the present results indicate doubly dissociated functional roles of the ventral striatum and the Arcopallium, the former in the cost of traveling for food and the latter in the cost of handling food, respectively.
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Differential distribution of L-aspartate- and L-glutamate-immunoreactive structures in the Arcopallium and medial striatum of the domestic chick (Gallus domesticus).
The Journal of comparative neurology, 2006Co-Authors: Ágota Ádám, András CsillagAbstract:The role of amino acid neurotransmitters in learning and memory is well established. We investigated the putative role of L-aspartate as a neurotransmitter in the arcopallial-medial striatal pathway, which is known to be involved in passive avoidance learning in domestic chicks. Double immunocytochemistry against L-aspartate and L-glutamate was performed at both light and electron microscopic levels. L-aspartate- and L-glutamate-immunoreactive neurons in the Arcopallium and posterior amygdaloid pallium were identified and counted by using fluorescence microscopy and confocal laser scanning microscopy. Most labeled neurons of Arcopallium were enriched in glutamate as well as aspartate. However, the Arcopallium and posterior amygdaloid pallium differed from a neighboring telencephalic region (nidopallium; formerly neostriatum) by containing a substantial proportion of cells singly labeled for L-aspartate (15%, vs. 5.3% in the nidopallium). Aspartate-labeled neurons constitute ∼20%, 25%, 42%, and 28% of total in the posterior amygdaloid pallium and the medial, dorsal, and anterior arcopallia, respectively. Immunoelectron microscopy showed that L-aspartate was enriched in terminals of the medial striatum. The labeled terminals had clear and round vesicles and asymmetric junctions; similar to those immunoreactive to L-glutamate. Axon terminals singly labeled for L-aspartate made up 17% of the total. In addition, 7% of neuronal perikarya and 26% of all dendritic profiles appeared to be labeled specifically with L-aspartate but not L-glutamate. The results indicate that L-aspartate may play a specific role (as distinct from that of L-glutamate) in the intrinsic and extrinsic circuits instrumental in avian learning and memory. J. Comp. Neurol. 498:266–276, 2006. © 2006 Wiley-Liss, Inc.
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localized lesions of ventral striatum but not Arcopallium enhanced impulsiveness in choices based on anticipated spatial proximity of food rewards in domestic chicks
Behavioural Brain Research, 2006Co-Authors: Naoya Aoki, András Csillag, Ryuhei Suzuki, Ei Ichi Izawa, Toshiya MatsushimaAbstract:The effects of bilateral chemical lesions of the ventral striatum (nucleus accumbens and the surrounding areas in the medial striatum) and Arcopallium (major descending area of the avian telencephalon) were examined in 1-2-weeks old domestic chicks. Using a Y-maze, we analyzed the lesion effects on the choices that subject chicks made in two tasks with identical economical consequences, i.e., a small-and-close food reward vs. a large-and-distant food reward. In task 1, red, yellow, and green beads were associated with a feeder placed at various distances from the chicks; chicks thus anticipated the spatial proximity of food by the bead's color, whereas the quantity of the food was fixed. In task 2, red and yellow flags on the feeders were associated with various amount of food; the chicks thus anticipated the quantity of food by the flag's color, whereas the proximity of the reward could be directly visually determined. In task 1, bilateral lesions of the ventral striatum (but not the Arcopallium) enhanced the impulsiveness of the chicks' choices, suggesting that choices based on the anticipated proximity were selectively changed. In task 2, similar lesions of the ventral striatum did not change choices. In both experiments, motor functions of the chicks remained unchanged, suggesting that the lesions did not affect the foraging efficiency, i.e., objective values of food. Neural correlates of anticipated food rewards in the ventral striatum (but not those in the Arcopallium) could allow chicks to invest appropriate amount of work-cost in approaching distant food resources.
Jacques Balthazart - One of the best experts on this subject based on the ideXlab platform.
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seasonal changes of perineuronal nets and song learning in adult canaries serinus canaria
Behavioural Brain Research, 2020Co-Authors: Gilles Cornez, Gregory F Ball, Clementine Collignon, Wendt Muller, Charlotte A Cornil, Jacques BalthazartAbstract:Abstract Songbirds learn their song during a sensitive period of development associated with enhanced neural plasticity. In addition, in open-ended learners such as canaries, a sensitive period for sensorimotor vocal learning reopens each year in the fall and leads to song modifications between successive breeding seasons. The variability observed in song production across seasons in adult canaries correlates with seasonal fluctuations of testosterone concentrations and with morphological changes in nuclei of the song control system (SCS). The sensitive periods for song learning during ontogeny and then again in adulthood could be controlled by the development of perineuronal nets (PNN) around parvalbumin-expressing interneurones (PV) which limits learning-induced neuroplasticity. However, this relationship has never been investigated in the context of adult vocal learning in adult songbirds. Here we explored PNN and PV expression in the SCS of adult male Fife Fancy canaries in relation to the seasonal variations of their singing behaviour. We found a clear pattern of seasonal variation in testosterone concentrations and song production. Furthermore, PNN expression was significantly higher in two specific song control nuclei, the robust nucleus of the Arcopallium (RA) and the Area X of the basal ganglia, during the breeding season and during the later stages of sensorimotor song development compared to birds in an earlier stage of sensorimotor development during the fall. These data provide the first evidence that changes in PNN expression could represent a mechanism regulating the closing-reopening of sensitive periods for vocal learning across seasons in adult songbirds.
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dissociable effects on birdsong of androgen signaling in cortex like brain regions of canaries
The Journal of Neuroscience, 2017Co-Authors: Gregory F Ball, Jacques Balthazart, Beau A AlwardAbstract:The neural basis of how learned vocalizations change during development and in adulthood represents a major challenge facing cognitive neuroscience. This plasticity in the degree to which learned vocalizations can change in both humans and songbirds is linked to the actions of sex steroid hormones during ontogeny but also in adulthood in the context of seasonal changes in birdsong. We investigated the role of steroid hormone signaling in the brain on distinct features of birdsong using adult male canaries ( Serinus canaria ), which show extensive seasonal vocal plasticity as adults. Specifically, we bilaterally implanted the potent androgen receptor antagonist flutamide in two key brain regions that control birdsong. We show that androgen signaling in the motor cortical-like brain region, the robust nucleus of the Arcopallium (RA), controls syllable and trill bandwidth stereotypy, while not significantly affecting higher order features of song such syllable-type usage (i.e., how many times each syllable type is used) or syllable sequences. In contrast, androgen signaling in the premotor cortical-like brain region, HVC (proper name), controls song variability by increasing the variability of syllable-type usage and syllable sequences, while having no effect on syllable or trill bandwidth stereotypy. Other aspects of song, such as the duration of trills and the number of syllables per song, were also differentially affected by androgen signaling in HVC versus RA. These results implicate androgens in regulating distinct features of complex motor output in a precise and nonredundant manner. SIGNIFICANCE STATEMENT Vocal plasticity is linked to the actions of sex steroid hormones, but the precise mechanisms are unclear. We investigated this question in adult male canaries ( Serinus canaria ), which show extensive vocal plasticity throughout their life. We show that androgens in two cortex-like vocal control brain regions regulate distinct aspects of vocal plasticity. For example, in HVC (proper name), androgens regulate variability in syntax but not phonology, whereas androgens in the robust nucleus of the Arcopallium (RA) regulate variability in phonology but not syntax. Temporal aspects of song were also differentially affected by androgen signaling in HVC versus RA. Thus, androgen signaling may reduce vocal plasticity by acting in a nonredundant and precise manner in the brain.
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Seasonal Plasticity in the Song Control System: Multiple Brain Sites of Steroid Hormone Action and the Importance of Variation in Song Behavior
Annals of the New York Academy of Sciences, 2004Co-Authors: Gregory F Ball, Lauren V. Riters, Catherine J. Auger, Daniel J. Bernard, Thierry Charlier, Jennifer J. Sartor, Jacques BalthazartAbstract:Birdsong, in non-tropical species, is generally more common in spring and summer when males sing to attract mates and/or defend territories. Changes in the volumes of song control nuclei, such as HVC and the robust nucleus of the Arcopallium (RA), are observed seasonally. Long photoperiods in spring stimulate the recrudescence of the testes and the release of testosterone. Androgen receptors, and at times estrogen receptors, are present in HVC and RA as are co-factors that facilitate the transcriptional activity of these receptors. Thus testosterone can act directly to induce changes in nucleus volume. However, dissociations have been identified at times among long photoperiods, maximal concentrations of testosterone, large song control nuclei, and high rates of song. One explanation of these dissociations is that song behavior itself can influence neural plasticity in the song system. Testosterone can act via brain-derived neurotrophic factor (BDNF) that is also released in HVC as a result of song activity. Testosterone could enhance song nucleus volume indirectly by acting in the preoptic area, a region regulating sexual behaviors, including song, that connects to the song system through catecholaminergic cells. Seasonal neuroplasticity in the song system involves an interplay among seasonal state, testosterone action, and behavioral activity.