Adult Male Zebra Finches Research Articles

A novel basal ganglia pathway forms a loop linking a vocal learning circuit with its dopaminergic input

Dopamine has been implicated in mediating contextual modulation of motor behaviors and learning in many species. In songbirds, dopamine may act on the basal ganglia nucleus Area X to influence the neural activity that contributes to vocal learning and contextual changes in song variability. Neurons in midbrain dopamine centers, the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA), densely innervate Area X and show singing-related changes in firing rate. In addition, dopamine levels in Area X change during singing. It is unknown, however, how song-related information could reach dopaminergic neurons. Here we report an anatomical pathway that could provide song-related information to the SNc and VTA. By using injections of bidirectionally transported fluorescent tracers in adult male zebra finches, we show that Area X and other song control nuclei do not project directly to the SNc or VTA. Instead, we describe an indirect pathway from Area X to midbrain dopaminergic neurons via a connection in the ventral pallidum (VP). Specifically, Area X projects to the VP via axon collaterals of Area X output neurons that also project to the thalamus. Dual injections revealed that the area of VP receiving input from Area X projects to the SNc and VTA. Furthermore, VP terminals in the SNc and VTA overlap with cells that project back to Area X. A portion of the arcopallium also projects to the SNc and VTA and could carry auditory information. These data demonstrate an anatomical loop through which Area X activity could influence its dopaminergic input.

What's That Sound? Auditory Area CLM Encodes Stimulus Surprise, Not Intensity or Intensity Changes

High-level sensory neurons encoding natural stimuli are not well described by linear models operating on the time-varying stimulus intensity. Here we show that firing rates of neurons in a secondary sensory forebrain area can be better modeled by linear functions of how surprising the stimulus is. We modeled auditory neurons in the caudal lateral mesopallium (CLM) of adult male zebra finches under urethane anesthesia with linear filters convolved not with stimulus intensity, but with stimulus surprise. Surprise was quantified as the logarithm of the probability of the stimulus given the local recent stimulus history and expectations based on conspecific song. Using our surprise method, the predictions of neural responses to conspecific song improved by 67% relative to those obtained using stimulus intensity. Similar prediction improvements cannot be replicated by assuming CLM performs derivative detection. The explanatory power of surprise increased from the midbrain through the primary forebrain and to CLM. When the stimulus presented was a random synthetic ripple noise, CLM neurons (but not neurons in lower auditory areas) were best described as if they were expecting conspecific song, finding the inconsistencies between birdsong and noise surprising. In summary, spikes in CLM neurons indicate stimulus surprise more than they indicate stimulus intensity features. The concept of stimulus surprise may be useful for modeling neural responses in other higher-order sensory areas whose functions have been poorly understood.

A Synaptic Basis for Auditory–Vocal Integration in the Songbird

Songbirds learn to sing by memorizing a tutor song that they then vocally mimic using auditory feedback. This developmental sequence suggests that brain areas that encode auditory memories communicate with brain areas for learned vocal control. In the songbird, the secondary auditory telencephalic region caudal mesopallium (CM) contains neurons that encode aspects of auditory experience. We investigated whether CM is an important source of auditory input to two sensorimotor structures implicated in singing, the telencephalic song nucleus interface (NIf) and HVC. We used reversible inactivation methods to show that activity in CM is necessary for much of the auditory-evoked activity that can be detected in NIf and HVC of anesthetized adult male zebra finches. Furthermore, extracellular and intracellular recordings along with spike-triggered averaging methods indicate that auditory selectivity for the bird's own song is enhanced between CM and NIf. We used lentiviral-mediated tracing methods to confirm that CM neurons directly innervate NIf. To our surprise, these tracing studies also revealed a direct projection from CM to HVC. We combined irreversible lesions of NIf with reversible inactivation of CM to establish that CM supplies a direct source of auditory drive to HVC. Finally, using chronic recording methods, we found that CM neurons are active in response to song playback and during singing, indicating their potential importance to song perception and processing of auditory feedback. These results establish the functional synaptic linkage between sites of auditory and vocal learning and may identify an important substrate for learned vocal communication.

Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia

The integration of two neural pathways generates learned song in zebra finches. The vocal motor pathway (VMP) is a direct connection between HVC (proper name) and the robust nucleus of the arcopallium (RA), whereas the anterior forebrain pathway (AFP) comprises an indirect circuit from HVC to RA that traverses the basal ganglia. Partial ablation (microlesion) of HVC in adult birds alters the integration of VMP and AFP synaptic input within RA and destabilizes singing. However, the vocal pattern shows surprising resilience because birds subsequently recover their song in approximately 1 week. Here, we show that deafening prevents vocal recovery after HVC microlesions, indicating that birds require auditory feedback to restore/relearn their vocal patterns. We then tested the role of the AFP (basal ganglia circuit) in this feedback-based recovery by ablating the output nucleus of the AFP [lateral magnocellular nucleus of the anterior nidopallium (LMAN)]. We found that LMAN ablation after HVC microlesions induced a sudden recovery of the vocal pattern. Thus, the AFP cannot be the neural locus of an instructive/learning mechanism that uses auditory feedback to guide vocal recovery, at least in this form of adult vocal plasticity. Instead, the AFP appears to be the source of the variable motor patterns responsible for vocal destabilization. In part, auditory feedback may restore song by strengthening the VMP component of synaptic input to RA relative to the AFP component.

Hemispheric Coordination Is Necessary for Song Production in Adult Birds: Implications for a Dual Role for Forebrain Nuclei in Vocal Motor Control

Precise coordination across hemispheres is a critical feature of many complex motor circuits. In the avian song system the robust nucleus of the arcopallium (RA) plays a key role in such coordination. It is simultaneously the major output structure for the descending vocal motor pathway, and it also sends inputs to structures in the brain stem and thalamus that project bilaterally back to the forebrain. Because all birds lack a corpus callosum and the anterior commissure does not interconnect any of the song control nuclei directly, these bottom-up connections form the only pathway that can coordinate activity across hemispheres. In this study, we show that unilateral lesions of RA in adult male zebra finches (Taeniopigia guttata) completely and permanently disrupt the bird's stereotyped song. In contrast, lesions of RA in juvenile birds do not prevent the acquisition of normal song as adults. These results highlight the importance of hemispheric interdependence once the circuit is established but show that one hemisphere is sufficient for complex vocal behavior if this interdependence is prevented during a critical period of development. The ability of birds to sing with a single RA provides the opportunity to test the effect of targeted microlesions in RA without confound of functional compensation from the contralateral RA. We show that microlesions cause significant changes in song temporal structure and implicate RA as playing a major part in the generation of song temporal patterns. These findings implicate a dual role for RA, first as part of the program generator for song and second as part of the circuit that mediates interhemispheric coordination.

Inhibition of injury‐induced glial aromatase reveals a wave of secondary degeneration in the songbird brain

Mechanical or anoxic/ischemic brain insult results in reactive gliosis and a pronounced wave of apoptotic secondary degeneration (WSD). Reactive glia express aromatase (estrogen synthase) and glial estrogen synthesis decreases apoptosis and the volume of degeneration. Whether aromatization by glia affects gliosis itself or the initiation/maintenance of the WSD remains unknown. Adult male zebra finches (Taeniopygia guttata) were injured with a needle that contained the aromatase inhibitor fadrozole or vehicle into contralateral hemispheres. Birds were killed at 0, 2, 6, 24, 72h, 2 or 6 weeks postinjury. Gliosis and degeneration were measured with vimentin- and Fluoro-Jade B-expression, respectively. Reactive gliosis was detectable at 6 h, reached asymptote at 72 h, and continued until 6 weeks postinsult. Gliosis extended further around fadrozole-injury than vehicle, an effect driven by a larger area of gliosis around fadrozole- relative to vehicle-injury at 72 h postinsult. Glial aromatase was inhibited for about 2 weeks postinjury since aromatase relative optical density was higher around fadrozole-injury relative to vehicle-injury until this time-point. Degeneration around vehicle-injury reached asymptote at 2 h postinsult, but that around fadrozole-injury peaked 24-72 h postinjury and decreased thereafter. Thus, the injury-induced WSD as described in mammals is detectable in zebra finches only following glial aromatase inhibition. In the zebra finch, injury-induced estrogen provision may decrease reactive gliosis and severely dampen the WSD, suggesting that songbirds are powerful models for understanding the role of glial aromatization in secondary brain damage.

The effect of social environment on singing behavior in the zebra finch ( Taeniopygia guttata) and its implication for neuronal recruitment

Previous studies found that complex social environment increases new neuronal recruitment in brains of adult male zebra finches, in comparison with exposure to a simple social environment. These experiments could not determine, however, whether this increase was due to greater amounts of auditory input (amount of auditory information the male is exposed to), or auditory output (amount of song it produces). To answer this question, we raised male zebra finches to adulthood in a controlled environment, and were then exposed them to either a single unfamiliar female (simple social environment) or to 45 unfamiliar zebra finches of both sexes (complex social environment). Their singing behavior was monitored in these new social environments. Birds which were exposed to a simple social environment sang significantly more than birds which were exposed to a complex social environment. This supports the hypothesis that increased neuronal recruitment in birds exposed to a complex social environment correlates with processing and storing of auditory input, and not with song produced by the bird.

Malignant melanoma in a zebra finch (Taeniopygia guttata): cytologic, histologic, and ultrastructural characteristics

An approximately 3-year-old adult male zebra finch (Taeniopygia guttata) was diagnosed with malignant melanoma. The large darkly pigmented tumor was located in the coelom, extended from the apex of the heart to the cloaca, and was adherent to the intestines and the ventriculus. Dark small masses (likely metastases) were observed in the lungs. Cytologically, the neoplasm consisted mainly of round to oval cells with brown or pale blue to blue-brown pigment. Lesser numbers of cells were stellate to dendritic with abundant amounts of brown pigment granules or were markedly pleomorphic with variable amounts of pigment. Histologically, the tumor consisted of dense sheets and aggregates of infiltrative melanocytes that were negative for S-100 and Melan A. A few cells were consistent with "signet-ring" melanocytes. Melanocytes examined by electron microscopy contained typical structures, mainly premelanosomes and melanosomes, of this cell type. However, melanocytes with marked pleomorphism also contained intracytoplasmic aggregates of filaments, consistent with previously reported ultrastructural findings in signet-ring or rhabdoid melanoma of nonavian species.

Pallidal Neuron Activity Increases during Sensory Relay through Thalamus in a Songbird Circuit Essential for Learning

Disinhibition of the thalamus remains the primary model of information transfer between the basal ganglia and the cortex. Yet in apparent conflict with this model, the globus pallidus, a GABAergic basal ganglia output structure, often exhibits marked increases in firing rate during movement. To investigate the translation of pallidal activity and its relay through the thalamus, we explored a basal ganglia-thalamic pathway essential for song learning in songbirds. We found that single units in the thalamic nucleus DLM of urethane-anesthetized adult male zebra finches responded selectively to playback of the bird's own song, like neurons in its upstream and downstream nuclei. Because the pallidal input to these neurons forms giant calyx-like synapses, we were able to record extracellular signals from these presynaptic terminals as well. Pallidal units were distinctly excited by song playback, suggesting an increase in GABAergic transmission in the thalamus during sensory processing. However, this overall increased firing rate was phasic, punctuated by rapid decelerations in firing rate. In several cases, we were able to record presynaptic and postsynaptic units simultaneously. Correlating the presynaptic and postsynaptic activity, we found that disinhibition of thalamus may entail pallidal firing rate decelerations rather than simple long pauses in spontaneous activity, as has long been assumed.

Auditory Plasticity in a Basal Ganglia-Forebrain Pathway during Decrystallization of Adult Birdsong

Adult male zebra finches maintain highly stable songs via auditory feedback. Prolonged exposure to distorted feedback may cause this stable (i.e., "crystallized") song to change its pattern, a process known as decrystallization. In the songbird, the telencephalic nucleus LMAN (lateral magnocellular nucleus of anterior nidopallium) is necessary for feedback-dependent song decrystallization, although whether and how electrophysiological properties of LMAN neurons change during decrystallization is unknown. In normal adult zebra finches, LMAN neurons exhibit highly selective responses to auditory presentation of the bird's own song (BOS), possibly providing a permanent referent for song maintenance. If so, LMAN neurons should maintain selectivity for the originally crystallized BOS after exposure to distorted feedback and during decrystallization. Alternatively, LMAN auditory selectivity in the adult may change during decrystallization. To distinguish between these possibilities, we sectioned the vocal nerve in adult male zebra finches, which spectrally distorted the birds' songs. Over the course of several weeks, experience of distorted feedback caused the song to decrystallize in a subset of birds. At various times after nerve section, electrophysiological recordings made under anesthesia revealed that auditory selectivity in LMAN could shift to the spectrally distorted song. Such auditory plasticity could be detected during the second week after nerve section, before the time birds typically decrystallized their songs. Moreover, all birds that underwent decrystallization at later times always manifested auditory plasticity in LMAN. To our knowledge, the present findings afford the first example of an electrophysiological correlate of song decrystallization.

Genomic resources for songbird research and their use in characterizing gene expression during brain development

Vocal learning and neuronal replacement have been studied extensively in songbirds, but until recently, few molecular and genomic tools for songbird research existed. Here we describe new molecular/genomic resources developed in our laboratory. We made cDNA libraries from zebra finch (Taeniopygia guttata) brains at different developmental stages. A total of 11,000 cDNA clones from these libraries, representing 5,866 unique gene transcripts, were randomly picked and sequenced from the 3' ends. A web-based database was established for clone tracking, sequence analysis, and functional annotations. Our cDNA libraries were not normalized. Sequencing ESTs without normalization produced many developmental stage-specific sequences, yielding insights into patterns of gene expression at different stages of brain development. In particular, the cDNA library made from brains at posthatching day 30-50, corresponding to the period of rapid song system development and song learning, has the most diverse and richest set of genes expressed. We also identified five microRNAs whose sequences are highly conserved between zebra finch and other species. We printed cDNA microarrays and profiled gene expression in the high vocal center of both adult male zebra finches and canaries (Serinus canaria). Genes differentially expressed in the high vocal center were identified from the microarray hybridization results. Selected genes were validated by in situ hybridization. Networks among the regulated genes were also identified. These resources provide songbird biologists with tools for genome annotation, comparative genomics, and microarray gene expression analysis.

Birdsong Memory: A Neural Dissociation between Song Recognition and Production

Songbirds learn their song from an adult conspecific tutor when they are young, much like the acquisition of speech in human infants. When an adult zebra finch is re-exposed to its tutor's song, there is increased neuronal activation in the caudomedial nidopallium (NCM), the songbird equivalent of the auditory association cortex. This neuronal activation is related to the fidelity of song imitation, suggesting that the NCM may contain the neural representation of song memory. We found that bilateral neurotoxic lesions to the NCM of adult male zebra finches impaired tutor-song recognition but did not affect the males' song production or their ability to discriminate calls. These findings demonstrate that the NCM performs an essential role in the representation of tutor-song memory. In addition, our results show that tutor-song memory and a motor program for the bird's own song have separate neural representations in the songbird brain. Thus, in both humans and songbirds, the cognitive systems of vocal production and auditory recognition memory are subserved by distinct brain regions.

HVC interneurons are not renewed in adult male zebra finches

Adult neurogenesis is a widespread phenomenon in many species, from invertebrates to humans. In songbirds, the telencephalic region, high vocal center (HVC), continuously integrates new neurons in adulthood. This nucleus consists of a heterogenous population of inhibitory interneurons (HVC(IN)) and two populations of projection neurons that send axons towards either the robust nucleus of the arcopallium (HVC(RA)) or the striatal nucleus area X (HVC(X)). New HVC neurons were initially inferred to be interneurons, because they lacked retrograde labelling from the HVC's targets. Later studies using different tracers demonstrated that HVC(RA) are replaced but HVC(X) are not. Whether interneurons are also renewed became an open question. As the HVC's neuronal populations display different physiological properties and functions, we asked whether adult HVC indeed recruits two neuronal populations or whether only the HVC(RA) undergo renewal in adult male zebra finches. We show that one month after being born in the lateral ventricle, 42% of the newborn HVC neurons were retrogradely labelled by tracer injections into the RA. However, the remaining 58% were not immunoreactive for the neurotransmitter GABA, nor for the calcium-binding proteins, parvalbumin (PA), calbindin (CB) and calretinin (CR) that characterize different classes of HVC(IN). We further established that simultaneous application of parvalbumin, calbindin and calretinin antibodies to HVC revealed approximately the same fraction of HVC neurons, i.e. 10%, as could be detected by GABA immunoreactivity. This implies that the sum of HVC(IN) expressing the different calcium-binding proteins constitute all inhibitory HVC(IN). Together these results strongly suggest that only HVC(RA) are recruited into the adult HVC.

Neuronal recruitment in adult zebra finch brain during a reproductive cycle

Previous studies suggest that adult neurogenesis and neuronal replacement are related to the acquisition of new information. The present study supports this hypothesis by showing that there is an increase in new neuron recruitment in brains of adult male and female zebra finches that coincides with the need to memorize vocalizations of nestlings before they fledge. We counted [(3)H]-Thymidine labeled neurons 40 days after [(3)H]-Thymidine injections. These counts were made in the parents' brains at the time eggs hatched, at the time juveniles fledged and still needed parental care, and at the time juveniles were already independent. We focused on nidopallium caudale (NC), a brain region which plays a role in sound processing. Recruitment of new NC neurons increased at the time the young fledged, followed by a significant decrease when the young reached independence. We suggest that this increase enables parents to recognize their own young when they are still dependent on parental feeding, yet easily lost among other fledglings in the colony. We saw no such increase in neuronal recruitment in the olfactory bulb, suggesting anatomical specificity for the effect seen in NC. We also found a preliminary, positive correlation between number of fledglings and number of new NC neurons in the parents' brain at fledging, suggesting that the number of neurons recruited is sensitive to the number of young fledged.

HVC microlesions do not destabilize the vocal patterns of adult male zebra finches with prior ablation of LMAN

The songs of adult male zebra finches (Taeniopygia guttata) arise by an integration of activity from two neural pathways that emanate from the telencephalic nucleus HVC (proper name). One pathway descends directly from HVC to the vocal premotor nucleus RA (the robust nucleus of the arcopallium) whereas a second pathway descends from HVC into a basal ganglia circuit (the anterior forebrain pathway, AFP) that also terminates in RA. Although HVC neurons that project directly to RA outnumber those that contribute to the AFP, both populations are distributed throughout HVC. Thus, partial ablation (microlesion) of HVC should damage both pathways in a proportional manner. We report here that bilateral HVC microlesions in adult male zebra finches produce an immediate loss of song stereotypy from which birds recover, in some cases within 3 days. The contribution of the AFP to the onset of song destabilization was tested by ablating the output nucleus of this circuit (LMAN, the lateral magnocellular nucleus of the anterior nidopallium) prior to bilateral HVC microlesions. Song stereotypy was largely unaffected. Together, our findings suggest that adult vocal production involves nonproportional integration of two streams of neural activity with opposing effects on song--HVC's direct projection to RA underlies production of stereotyped song whereas the AFP seems to facilitate vocal variation. However, the rapid recovery of song in birds with HVC microlesions alone suggests the presence of dynamic corrective mechanisms that favor vocal stereotypy.

Dynamic Role of Postsynaptic Caspase-3 and BIRC4 in Zebra Finch Song-Response Habituation

Activation of the protease caspase-3 is commonly thought to cause apoptotic cell death. Here, we show that caspase-3 activity is regulated at postsynaptic sites in brain following stimuli associated with memory (neural activation and subsequent response habituation) instead of cell death. In the zebra finch auditory forebrain, the concentration of caspase-3 active sites increases briefly within minutes after exposure to tape-recorded birdsong. With confocal and immunoelectron microscopy, we localize the activated enzyme to dendritic spines. The activated caspase-3 protein is present even in unstimulated brain but bound to an endogenous inhibitor, BIRC4 (xIAP), suggesting a mechanism for rapid release and sequestering at specific synaptic sites. Caspase-3 activity is necessary to consolidate a persistent physiological trace of the song stimulus, as demonstrated using pharmacological interference and the zenk gene habituation assay. Thus, the brain appears to have adapted a core component of cell death machinery to serve a unique role in learning and memory.

Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds.

In both humans and songbirds, infants learn vocalizations by imitating the sounds of adult tutors with whom they interact during an early sensitive period. Vocal learning occurs in few animal taxa; similarities in the imitation process between humans and songbirds make the songbird a unique system in which vocal learning mechanisms can be studied at the neurobiological level. One theory of vocal learning proposes that early auditory experience generates auditory memories that subsequently guide vocal imitation. We now present a combination of behavioral and neurophysiological results, obtained in a songbird, that support this theory. We show that neurons in a forebrain auditory area of adult male zebra finches are selectively tuned to the song of a tutor heard early in development. Furthermore, the strength of this selectivity shows a striking correlation with the fidelity of vocal imitation, suggesting that this auditory memory may have served as the model for song learning.

HVC microlesions do not destabilize the vocal patterns of adult male zebra finches with prior ablation of LMAN

The songs of adult male zebra finches (Taeniopygia guttata) arise by an integration of activity from two neural pathways that emanate from the telencephalic nucleus HVC (proper name). One pathway descends directly from HVC to the vocal premotor nucleus RA (the robust nucleus of the arcopallium) whereas a second pathway descends from HVC into a basal ganglia circuit (the anterior forebrain pathway, AFP) that also terminates in RA. Although HVC neurons that project directly to RA outnumber those that contribute to the AFP, both populations are distributed throughout HVC. Thus, partial ablation (microlesion) of HVC should damage both pathways in a proportional manner. We report here that bilateral HVC microlesions in adult male zebra finches produce an immediate loss of song stereotypy from which birds recover, in some cases within 3 days. The contribution of the AFP to the onset of song destabilization was tested by ablating the output nucleus of this circuit (LMAN, the lateral magnocellular nucleus of the anterior nidopallium) prior to bilateral HVC microlesions. Song stereotypy was largely unaffected. Together, our findings suggest that adult vocal production involves nonproportional integration of two streams of neural activity with opposing effects on song—HVC's direct projection to RA underlies production of stereotyped song whereas the AFP seems to facilitate vocal variation. However, the rapid recovery of song in birds with HVC microlesions alone suggests the presence of dynamic corrective mechanisms that favor vocal stereotypy. © 2006 Wiley Periodicals, Inc. Develop Neurobiol 67: 205–218, 2007.

Noradrenergic Modulation of Activity in a Vocal Control Nucleus In Vitro

Norepinephrine (NE) can profoundly modulate sensory processing, but its effect on motor function is less well understood. Birdsong is a learned behavior involving sensory and motor processes that are influenced by NE. A potential site of NE action is the robust nucleus of the arcopallium (RA): RA receives noradrenergic inputs and has adrenergic receptors, and it is a sensorimotor area instrumental to song production. We hypothesized that NE modulates RA neurons, and as a first test, we examined the effect of NE on RA activity in vitro. We recorded spontaneous activity extracellularly from isolated RA neurons in brain slices made from adult male zebra finches. These neurons exhibited regular tonic activity with firing rates averaging 5.5 Hz. Bath application of NE rapidly and reversibly decreased firing for the majority of neurons, to the extent that spontaneous activity was often abolished. This was likely a direct effect on the cell recorded, because it occurred with blockade of fast excitatory and inhibitory synaptic transmission or of all synaptic transmission. The NE-induced suppression involved alpha2-adrenergic receptors: yohimbine, an antagonist, completely reversed the suppression, and clonidine, an agonist, partially mimicked it. Perforated patch recordings revealed that NE induced a conductance increase in RA neurons; however, this did not prevent cells from firing when stimulated by afferents in HVC. For some neurons, NE application resulted in an increase in signal-to-noise ratio for spikes evoked by HVC stimulation. Thus NE could strongly modulate the spontaneous activity of RA cells, potentially enhancing signals relayed through RA.

Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song

Male songbirds typically require exposure to normal adult conspecific song during development in order to learn a normal song of their own. Females require exposure to conspecific song during development in order to select high-quality, learned song over the incomplete song produced by males reared in isolation. Altering males' opportunity for song learning during development affects the neuroanatomy of brain regions involved in song production (the song system), but in females the neural effects of song learning are unknown. We raised male and female zebra finches (Taeniopygia guttata) with differing amounts of exposure to singing males during development. At 120 days, we Golgi-stained their brains and measured the frequency of dendritic spines in brain areas used in song perception or production. We found that females reared with little or no exposure to song have 31% fewer dendritic spines per unit length of dendrite in caudomedial nidopallium (NCM), a brain area activated by song perception, compared to control females. The deprived females had small deficits in the frequency of spines in HVC, a region activated by song production in males. Males with limited exposure to song had a 24% lower spine density in HVC than controls but only a 10% lower density in NCM. These data support the hypothesis that NCM is important in auditory learning, while HVC is involved in sensorimotor learning, and that these capacities are differentially emphasized in the two sexes.