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Biomedical subjects

F Nottebohm

Publications and source records attributed to F Nottebohm.

At least 19 recordsLinked to original sources

Social inhibition of song imitation among sibling male zebra finches.

A male zebra finch, Taeniopygia guttata, kept with its father until adulthood develops an imitation of its father's song motif. We report here that the completeness of this imitation was sensitive to the social or auditory context in which the bird grew up: the greater the number of male siblings in a clutch, the shorter the mean duration of the song motif and the fewer the mean number of song notes imitated from the father; the latter shortfall was not compensated by other, improvised notes. We call this effect fraternal inhibition. Fraternal inhibition was avoided by members of a clutch that developed the song first. To our surprise, this role commonly fell to one of the younger birds in the clutch. Early song learning may influence fitness since individuals that produced the most complete imitations also tended to induce more egg laying.

Animal Communication

Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata).

Here, we examine the connectivity of two previously identified telencephalic stations of the auditory system of adult zebra finches, the neostriatal "shelf" that underlies the high vocal center (HVC) and the archistriatal "cup" adjacent to the robust nucleus of the archistriatum (RA). We used different kinds of neuroanatomical tracers to visualize the projections from the shelf to the HVC. In addition, we show that the shelf projects to the cup and that the cup projects to thalamic, midbrain, and pontine nuclei of the ascending auditory pathway. Our observations extend to songbirds anatomical features that are found in the auditory pathways of a nonoscine bird, the pigeon (Wild et al. [1993] J. Comp. Neurol. 337:32-62), and we suggest that the descending auditory projections found in mammals may also be a general property of the avian brain. Finally, we show that the oscine song control system is closely apposed to auditory pathways at many levels. Our observations may help in understanding the evolution and organization of networks for vocal communication and vocal learning in songbirds.

Animals

Context determines the sex appeal of male zebra finch song.

We explored the conditions under which playbacks of male zebra finch, Taeniopygia guttata, song induced reproduction in females. In a laboratory study, a rise in faecal oestrogen levels predicted egg laying. Song playbacks by themselves induced a decrease in oestrogen levels. There was an increase in oestrogen levels, followed by egg laying, when the song was broadcast from inside a male model positioned away from the nest. However, this effect occurred only when a second, silent male model was perched on the rim of the nest. If song was broadcast from inside the model perched on the nest, there was no increase in oestrogen levels. We conclude that tests of song efficacy in female songbirds must respect some contextual rules, which are likely to vary between species. Only then does it become possible to ascertain which sounds are most effective in inducing physiological changes leading to reproduction. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article

For whom the bird sings: context-dependent gene expression.

Male zebra finches display two song behaviors: directed and undirected singing. The two differ little in the vocalizations produced but greatly in how song is delivered. "Directed" song is usually accompanied by a courtship dance and is addressed almost exclusively to females. "Undirected" song is not accompanied by the dance and is produced when the male is in the presence of other males, alone, or outside a nest occupied by its mate. Here, we show that the anterior forebrain vocal pathway contains medial and lateral "cortical-basal ganglia" subdivisions that have differential ZENK gene activation depending on whether the bird sings female-directed or undirected song. Differences also occur in the vocal output nucleus, RA. Thus, although these two vocal behaviors are very similar, their brain activation patterns are dramatically different.

Animals

Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway.

Adult zebra finches can produce normal song in the absence of Area X, IMAN, or DLM, nuclei that constitute the anterior forebrain pathway of songbirds. Here, we address whether lesions involving Area X and IMAN affect adult male zebra finches' ability to discriminate between conspecific or heterospecific songs. Intact birds and lesioned birds were trained on an operant GO/NOGO conditioning paradigm to discriminate between hetero- or conspecific songs. Both lesioned and intact birds were able to learn all discriminations. Lesioned and intact birds performed equivalently on canary song discriminations. In contrast, discriminations involving bird's own song took significantly more trails to learn for lesioned birds than for intact birds. Discrimination between conspecific songs in general also took longer in the lesioned birds, but missed significance level. Birds with control lesions medial to Area X did not show any differences from intact animals. Our results suggest that an intact anterior forebrain pathway is not required to discriminate between heterospecific songs. In contrast, Area X and IMAN contribute to a male zebra finch's ability to discriminate between its own song and that of other zebra finches.

Animals

Selective expression of insulin-like growth factor II in the songbird brain.

Neuronal replacement occurs in the forebrain of juvenile and adult songbirds. To address the molecular processes that govern this replacement, we cloned the zebra finch insulin-like growth factor II (IGF-II) cDNA, a factor known to regulate neuronal development and survival in other systems, and examined its expression pattern by in situ hybridization and immunocytochemistry in juvenile and adult songbird brains. The highest levels of IGF-II mRNA expression occurred in three nuclei of the song system: in the high vocal center (HVC), in the medial magnocellular nucleus of the neostriatum (mMAN), which projects to HVC, and to a lesser extent in the robust nucleus of the archistriatum (RA), which receives projections from HVC. IGF-II mRNA expression was developmentally regulated in zebra finches. In canary HVC, monthly changes in IGF-II mRNA expression covaried with previously reported monthly differences in neuron incorporation. Combining retrograde tracers with in situ hybridization and immunocytochemistry, we determined that the HVC neurons that project to area X synthesize the IGF-II mRNA, whereas the adjacent RA-projecting neurons accumulate the IGF-II peptide. Our findings raise the possibility that within HVC IGF-II acts as a paracrine signal between nonreplaceable area X-projecting neurons and replaceable RA-projecting neurons, a mode of action that is compatible with the involvement of IGF-II with the replacement of neurons. Additional roles for IGF-II expression in songbird brain are likely, because expression also occurs in some brain areas outside the song system, among them the cerebellar Purkinje cells in which neurogenesis is not known to occur.

Amino Acid Sequence

Expression of brain lipid binding protein in the brain of the adult canary and its implications for adult neurogenesis.

Brain lipid binding protein (BLBP), a member of the fatty acid binding protein family, is expressed at high levels in the mammalian central nervous system during development, but not in adulthood. Because the brain of adult birds continues to show significant levels of neurogenesis, we thought it likely that BLBP expression would also be present. We used a polyclonal antibody against BLBP to study the presence of this protein in the adult canary brain. This antibody stained 1) fibers and perikarya of radial cells in the telencephalon; 2) Bergmann glia in the cerebellum; 3) astrocytes; 4) tanicytes in the walls of the third ventricle; 5) the neuropil of certain forebrain and brainstem regions, including nuclei of the song system; and 6) some migrating cells in the telencephalon. This anatomical distribution suggests that BLBP plays a role in the neuronal migration and synaptic reorganization of adult avian brain.

Aging

Motor-driven gene expression.

There is increased neuronal firing in the high vocal center (a motor nucleus) and other song nuclei of canaries, Serinus canaria, and zebra finches, Taeniopygia guttata, whenever these songbirds sing or hear song. These observations suggested that song perception involved sensory and motor pathways. We now show that the act of singing, but not hearing song, induces a rapid and striking increase (up to 60-fold) in expression of the transcriptional regulator ZENK in the high vocal center and other song nuclei. This motor-driven gene expression is independent of auditory feedback, since it occurs in deafened birds when they sing and in muted birds when they produce silent song. Conversely, hearing song, but not the act of singing, induces ZENK expression in parts of the auditory forebrain. Our observations show that even though the same auditory stimulus activates sensory and motor pathways, perception and production of song are accompanied by anatomically distinct patterns of gene expression.

Animals

Reafferent thalamo- "cortical" loops in the song system of oscine songbirds.

Songbirds have a complex vocal repertoire, much of which is learned by imitation. The vocal motor system of songbirds includes a set of telencephalic pathways dedicated to the acquisition and production of learned song. The main vocal motor pathway goes from the high vocal center (HVC) to the robust nucleus of the archistriatum (RA), which in turn innervates mesencephalic and medullary nuclei involved in vocalization. We used neural tract tracers (biotinylated dextran amines, fluorescein- and rhodamine-linked dextran amines, and Fluorogold) to show that RA of adult male canaries (Serinus canaria) and zebra finches (taeniopygia guttata) sends an ipsilateral projection to the posterior portion of the dorsomedial thalamic nucleus (DMP). DMP projects to the medial portion of the magnocellular nucleus of the anterior neostriatum (mMAN), which is known to project to HVC, forming a feedback circuit. We also observed that the projection from DMP to mMAN is bilateral. Extracellular multi-unit recordings from awake restrained subjects have demonstrated that mMAN has auditory responses that are selective for the bird's own song. These auditory responses are similar to responses recorded simultaneously in HVC, but with a longer latency, suggesting that mMAN receives auditory information from HVC through the circuit we have described. We also saw a weaker projection from RA to the medial part of the dorsolateral nucleus of the thalamus (DLM), which is known to project to the lateral portion of the magnocellular nucleus of the anterior neostriatum (IMAN). IMAN is known to project to RA, completing yet another feedback circuit; IMAN is also part of the anterior forebrain pathway, which plays an essential role in song learning. These thalamo-telencephalic circuits are similar to the thalamo-cortical circuits found in mammalian motor systems, and we suggest that the signals carried by these loops may be important for song perception, song learning, song production, and/or the bilateral coordination of vocal motor commands.

Afferent Pathways

Quantal duration of auditory memories.

Neuronal responses in the caudomedial neostriatum (NCM) of adult zebra finches (Taeniopygia guttata) decreased upon repeated, unreinforced presentations of conspecific song, calls, or other complex sounds. This "stimulus-specific habituation" is a form of learning, and its spontaneous loss, a form of "forgetting." Spontaneous forgetting occurred only at narrowly defined times (2 to 3, 6 to 7, 14 to 15, 17 to 18.5, 46 to 48, or 85 to 89 hours after first exposure to a stimulus), determined by stimulus class, number of presentations, and interval between presentations. The first five forgetting times coincided with periods when gene expression and protein synthesis in NCM were required for maintenance of the longer lasting (85 to 89 hours) habituation. The number of successive episodes of gene expression induced by a stimulus, but occurring long after stimulus presentation, appears to determine the quantal duration of auditory memories.

Acoustic Stimulation

Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches.

Auditory information is critical for vocal imitation and other elements of social life in song birds. In zebra finches, neural centers that are necessary for the acquisition and production of learned vocalizations are known, and they all respond to acoustic stimulation. However, the circuits by which conspecific auditory signals are perceived, processed, and stored in long-term memory have not been well documented. In particular, no evidence exists of direct connections between auditory and vocal motor pathways, and two newly identified centers for auditory processing, caudomedial neostriatum (Ncm) and caudomedial hyperstriatum ventrale (cmHV), have no documented place among known auditory circuits. Our goal was to describe anatomically the auditory pathways in adult zebra finch males and, specifically, to show the projections by which Ncm and vocal motor centers may receive auditory input. By using injections of different kinds of neuroanatomical tracers (biotinylated dextran amines, rhodamine-linked dextran amines, biocytin, fluorogold, and rhodamine-linked latex beads), we have shown that, as in other avian groups, the neostriatal field L complex in caudal telencephalon is the primary forebrain relay for pathways originating in the auditory thalamus, i.e., the nucleus ovoidalis complex (Ov). In addition, Ncm and cmHV also receive input from the Ov complex. Ov has been broken down into two parts, the Ov "core" and "shell," which project in parallel to different targets in the caudal telencephalon. Parts of the field L complex are connected among themselves and to Ncm, cmHV, and caudolateral Hv (clHV) through a complex web of largely reciprocal pathways. In addition, clHV and parts of the field L complex project strongly to the "shelf" of neostriatum underneath the song control nucleus high vocal center (HVC) and to the "cup" of archistriatum rostrodorsal to another song-control nucleus, the robust nucleus of the archistriatum (RA). We have documented two points at which the vocal motor pathway may pick up auditory signals: the HVC-shelf interface and a projection from clHV to the nucleus interfacialis (NIf), which projects to HVC. These data represent the most complete survey to date of auditory pathways in the adult male zebra finch brain, and of their projections to motor stations of the song system.

Acoustic Stimulation

A large-capacity memory system that recognizes the calls and songs of individual birds.

Auditory responses in the caudomedial neostriatum (NCM) of the zebra finch (Taeniopygia guttata) forebrain habituate to repeated presentations of a novel conspecific song. This habituation is long lasting and specific to individual stimuli. We here test the acoustic and ethological basis of this stimulus-specific habituation by recording extracellular multiunit activity in the NCM of awake male and female zebra finches presented with a variety of conspecific and heterospecific vocalizations, white noise, and tones. Initial responses to conspecific song and calls and to human speech were higher than responses to the other stimuli. Immediate habituation rates were high for all novel stimuli except tones, which habituated at a lower rate. Habituation to conspecific calls and songs outlasted habituation to other stimuli. The extent of immediate habituation induced by a particular novel song was not diminished when other conspecific songs were presented in alternation. In addition, the persistence of habituation was not diminished by exposure to other songs before testing, nor was it influenced by gender or laterality. Our results suggest that the NCM is specialized for remembering the calls and songs of many individual conspecifics.

Animals

Expression of polysialylated N-CAM in the central nervous system of adult canaries and its possible relation to function.

Polysialylated neuronal cell adhesion molecule (PSA-N-CAM) is a cell surface molecule associated with neurons that undergo changes in configuration or spatial translocation. In both cases, this molecule is thought to reduce the adhesivity of these cells or of their processes, which can thereby insinuate themselves into the existing parenchyma. We used a monoclonal antibody specific to PSA to offer what we believe is the first account of the distribution of PSA-N-CAM in the adult songbird brain. This antibody stained a diversity of cell classes and processes, as follows: 1) a subset of ventricular zone cells; 2) migrating cells thought to be neuroblasts; 3) a subset of differentiated neurons; 4) some brain surface astrocytes; 5) some tanycytes; 6) the neuropil of some regions; 7) some axonal fibers; and 8) possibly some synapses. Our results demonstrate also, for the first time, the wide distribution of a very numerous population of migrating cells in the telencephalon and the seasonal regulation of PSA-N-CAM expression in a part of the adult brain known to undergo seasonal changes in cell recruitment and function. However, we did not find PSA-N-CAM associated with young migrating cells in the high vocal center (HVC), nor was there PSA-N-CAM in the robust nucleus of the archistriatum (RA), which is known to receive new axonal endings from HVC. In these instances spatial translocation may occur with the assistance of other surface molecules.

Animals

Feedback circuitry within a song-learning pathway.

The song system of birds consists of several neural pathways. One of these, the anterior forebrain pathway, is necessary for the acquisition but not for the production of learned song in zebra finches. It has been shown that the anterior forebrain pathway sequentially connects the following nuclei: the high vocal center, area X of lobus parolfactorius, the medial portion of the dorsolateral thalamic nucleus, the lateral magnocellular nucleus of anterior neostriatum (IMAN), and the robust nucleus of the archistriatum (RA). We now show in zebra finches (Taeniopygia guttata) that IMAN cells that project to RA also project to area X, forming a feedback loop within the anterior forebrain pathway. The axonal endings of the IMAN projection into area X form cohesive and distinct domains. Small injections of tracer in subregions of area X backfill a spatially restricted subset of cells in IMAN, that, in turn, send projections to RA that are arranged in horizontal layers, which may correspond to the functional representation of vocal tract muscles demonstrated by others. We infer from our data that there is a myotopic representation throughout the anterior forebrain pathway. In addition, we suggest that the parcellation of area X into smaller domains by the projection from IMAN highlights a functional architecture within X, which might correspond to units of motor control, to the representation of acoustic features of song, or both.

Animals

Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain.

Earlier work showed that playbacks of conspecific song induce expression of the immediate early gene ZENK in the caudo-medial neostriatum (NCM) of awake male zebra finches and that this response disappears with repeated presentations of the same stimulus. In the present study, we investigated whether repetitions of a song stimulus also elicited a decrement in the electrophysiological responses in the NCM neurons of these birds. Multiunit auditory responses in NCM were initially vigorous, but their amplitude decreased (habituated) rapidly to repeated stimulation, declining to about 40% of the initial response during the first 50 iterations. A similar time course of change was seen at the single unit level. This habituation occurred specifically for each song presented but did not occur when pure tones were used as a stimulus. Habituation to conspecific, but not heterospecific, song was retained for 20 h or longer. Injections of inhibitors of protein or RNA synthesis at the recording site did not affect the initial habituation to a novel stimulus, but these drugs blocked the long-term habituation when injected at 0.5-3 h and at 5.5-7 h after the first exposure to the stimulus. Thus, at least two waves of gene induction appear to be necessary for long-lasting habituation to a particular song.

Acoustic Stimulation

Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon.

Conspecific song induces a prompt increase in the expression of the zenk gene in the caudo-medial neostriatum (NCM), a part of the auditory telencephalon of songbirds. To test the hypothesis that zenk gene induction in NCM is related to the acquisition of new song-related memories, we presented adult male zebra finches with repeated playbacks of one song. In response, zenk mRNA levels in NCM increased for the first 30 min, but then declined back to baseline levels despite continued stimulation with the same song. When a novel song was then introduced, however, a full zenk response was triggered once again. Even when a full day had passed between the last exposure to a song and the testing period, the song that had been rendered "familiar" by repetition caused no zenk response, whereas a novel song caused a full response. Quantitative analysis indicates that individual cells in NCM must have undergone a selective loss in their zenk responsiveness to the repeated song, while still maintaining their ability to respond to the novel song. These results support the hypothesis that the induction of zenk is related to the formation of long-term memories. Analysis of the stimulus-specific modulation of zenk responses, coupled with appropriate behavioral assays, should provide insight into neural mechanisms responsible for the discrimination and storage of complex perceptual information.

Animal Communication