Quantal memory durations: observations not reproduced.
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Animals↗
Biomedical subjects
D S Vicario
Publications and source records attributed to D S Vicario.
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↗
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↗
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↗
Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds.
1. Microstimulation (trains of biphasic current pulses at 50-400 Hz lasting 2-4 s) was delivered unilaterally to known vocal control areas in the brains of zebra finches and canaries to elicit vocalizations. 2. Simple vocalizations were elicited from the midbrain, and the lowest thresholds were obtained from the dorsomedial nucleus of the intercollicular complex (DM). 3. Vocalizations elicited from forebrain vocal control nuclei higher vocal center (HVC) and robustus archistriatalis (RA) were complex, with features specific not only to the species, but to the individual bird's own learned song. 4. Complex acoustic features depended on innervation of the bird's vocal organ and were lost when the tracheosyringeal nerve was cut. 5. We suggest that stimulation of the forebrain vocal pathway activates a dedicated neural circuit that generates the temporal structure of song and whose specific pattern of activity is programmed during sensorimotor learning in each individual.
Animals↗
Motor mechanisms relevant to auditory-vocal interactions in songbirds.
Vocal learning through imitation underlies both human speech acquisition and song acquisition in oscine birds; both processes depend on auditory information. In songbirds, a specialized forebrain pathway is responsible for producing the learned temporal and acoustic features of vocalizations, and auditory input reaches every level of this pathway. Nucleus robustus archistriatalis (RA) is the source of the final common output from this pathway; RA is topographically organized into subregions that control the syringeal, respiratory and other effectors involved in vocal production. The acoustic features of learned vocalizations are primarily produced by specific patterns and combinations of syringeal muscle activity, while the overall temporal structure is primarily under respiratory control. In RA, and other vocal control structures, the individual bird's own learned song (BOS) is the most effective stimulus for eliciting auditory responses. Some neurons are 'combination-selective' in that they respond maximally to stimuli consisting of sequences of syllables from song. The recording sites that respond selectively to BOS tend to be located in more ventral parts of RA, the subregion that projects to motor neurons controlling syringeal muscles. These observations do not distinguish between motor feedback and perceptual hypotheses about the function of auditory responses in vocal motor pathways but are consistent with the idea that such responses may reflect a specific pattern of interaction between sensory and motor events that reflects vocal learning.
Animals↗
Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch.
Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to respond to sound stimuli. The auditory responses in one such nucleus, robustus archistriatalis (RA), were characterized by making multi-unit recordings in awake and anesthetized adult male zebra finches and in birds that had received lesions of the input to RA from the lateral part of the magnocellular nucleus of the anterior neostriatum (LMAN) or the Higher Vocal Center (HVC). In awake birds, RA neurons have a high level of spontaneous activity and vigorous auditory responses to song stimuli. Significantly greater responses are seen to the bird's own song (BOS) than to BOS played in reverse (REV) or to the songs of conspecifics (CON). Under ketamine-xylazine anesthesia, spontaneous activity is reduced, response latency increases and responses to BOS, REV and CON are indistinguishable. Responses obtained under urethane anesthesia are similar to those seen in awake birds. Thus, the pattern and selectivity of auditory responses in RA depend on the animal's state. Auditory responses in RA are qualitatively unchanged following lesion of the input to RA from LMAN, indicating that this pathway is not required for the sensory processing that underlies the preference for BOS on the vocal production pathway. Our results show that an input other than that from LMAN must be primarily responsible for auditory responses in RA. The direct projection from HVC is the most likely pathway by which song selective auditory information arrives in RA, since lesioning HVC abolished auditory responses in RA.
Animals↗
Temporal patterning of song production: participation of nucleus uvaeformis of the thalamus.
Birdsong is a learned vocal behavior used in intraspecific communication. The motor pathway serving learned vocalizations includes the forebrain nuclei NIf, HVC, and RA; RA projects to midbrain and brain stem areas that control the temporal and acoustic features of song. Nucleus Uvaeformis of the thalamus (Uva) sends input to two of these forebrain nuclei (NIf and HVC) but has not been thought to be important for song production. We used three experimental approaches to reexamine Uva's function in adult male zebra finches. (1) Electrical stimulation applied to Uva activated HVC and the vocal motor pathway, including tracheosyringeal motor neurons that innervate the bird's vocal organ. (2) Bilateral lesions of Uva including the dorso-medial portion of the nucleus affected the normal temporal organization of song. (3) Chronic multiunit recordings from Uva during normal song and calls show bursts of premotor activity that lead the onset of some song components, and also larger bursts that mark the end of complete song motifs. These results implicate Uva in the production of learned vocalizations, and further suggest that Uva contributes more to the temporal structure than to the acoustic characteristics of song.
Animals↗
A new brain stem pathway for vocal control in the zebra finch song system.
Projections from the telecephalic vocal control nucleus robustus archistriatalis (RA) to the brain stem were studied with anterograde and retrograde tracers in adult male Zebra finches. A previously undescribed projection to the ventrolateral medulla that originates in a dorsal subregion of the RA was found, in addition to the known projections to the tracheosyringeal portion of the hypoglossal nucleus (nXIIts) and to the dorsomedial nucleus of the intercollicular complex (DM), a mesencephalic vocal area. The DM was also found to project to the same area of the lateral medulla, which in turn projects to the nXIIts. This area in the lateral medulla includes the nucleus ambiguus, and may be of a pathway that links the telencephalic vocal pathway with respiratory control areas.
Animals↗
Song presentation induces gene expression in the songbird forebrain.
We investigated the participation of genomic regulatory events in the response of the songbird brain to a natural auditory stimulus of known physiological and behavioral relevance, birdsong. Using in situ hybridization, we detected a rapid increase in forebrain mRNA levels of an immediate-early gene encoding a transcriptional regulator (ZENK; also known as zif-268, egr-1, NGFI-A, or Krox-24) following presentation of tape-recorded songs to canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). ZENK induction is most marked in a forebrain region believed to participate in auditory processing and is greatest when birds hear the song of their own species. A significantly lower level of induction occurs when birds hear the song of a different species and no induction is seen after exposure to tone bursts. Cellular analysis indicates that the level of induction reflects the proportion of neurons recruited to express the gene. These results suggest a role for genomic responses in neural processes linked to song pattern recognition, discrimination, or the formation of auditory associations.
Acoustic Stimulation↗
Organization of the zebra finch song control system: II. Functional organization of outputs from nucleus Robustus archistriatalis.
The organization of projections from nucleus robustus archistriatalis (RA) was mapped by a combination of anatomical tracer techniques. After injections of retrograde tracers in the syringeal part of the hypoglossal motor nucleus (nXIIts), labelled cells were seen in ipsilateral RA, in agreement with previous work. However, a shallow band in the dorsal and dorsocaudal part of RA did not contain labelled cells. Cells in this "cap" area were labelled following tracer injections in the dorsomedial nucleus of midbrain ICo (DM), the other known target of RA projections. The topography of outputs to nXIIts was further examined by making small injections of retrograde tracer into physiologically identified control zones for individual syringeal muscles in nXIIts. The distribution of labelled cells in RA revealed bands of cells that cross RA in approximately horizontal layers and project to different parts of nXIIts. This topography was confirmed with the anterograde tracer PHA-L. Thus RA contains two functional subdivisions, one related to midbrain centers for vocalization and the other directly controlling syringeal motorneurons. The latter area can be further divided into zones that preferentially engage particular syringeal muscles.
Animals↗
Contributions of syringeal muscles to respiration and vocalization in the zebra finch.
Acute and chronic electromyographic (EMG) recordings from individual syringeal muscles were used to study syringeal participation in respiration and vocalization. In anesthetized birds, all syringeal muscles recorded were active to some degree during the expiratory phase of respiration, following activity in the abdominal musculature and preceding the emergence of breath from the nostril. In awake birds, the ventralis (V) muscle fired a strong, consistent burst, but the dorsalis (D) was variable both in strength and timing. Denervation of V is sufficient to produce the wheezing respiration originally seen in birds with complete bilateral section of the tracheosyringeal nerve. Complete syringeal denervation also removed almost all the acoustic features that distinguish individual song syllables, but had a minor effect on the temporal structure of song. When activity in V and D was recorded in awake, vocalizing birds, D was active before and during sound production, and V showed a small burst before sound onset and a vigorous burst timed to the termination of sound. During song, V was consistently active at sound offset, but also participated during sound for narrow bandwidth syllables. For some syllables (simple harmonic stacks), neither muscle was active. These data suggest that V contributes to syllable termination during vocalization and may silence the syrinx during normal respiration. D contributes to the acoustic structure of most syllables, and V may contribute to a special subset of syllables. In summary, the syringeal muscles show different activity patterns during respiration and vocalization and can be independently activated during vocalization, depending on the syllable produced.
Animals↗
Early estrogen treatment alone causes female zebra finches to produce learned, male-like vocalizations.
The male zebra finch produces learned song and long calls while the female does not. This difference in behavior is believed to result from the action of sex steroids on brain areas responsible for vocal production and learning. In this study, the female zebra finch was used to explore further the specific role sex steroids play in vocal masculinization. We show that estradiol (E2) treatment at birth was sufficient to masculinize the vocal behavior of female zebra finches. Thirteen of 18 females treated with E2 as nestlings produced song-like vocalizations. Fifteen of 18 produced long calls with male-typical features. The degree of masculinization varied between individuals. Of the 15 early E2 females that produced at least one type of male-like vocalization, 7 showed evidence of vocal learning from their tutors. The ability of E2 to cause masculinization of vocal behavior was age dependent: treatment from birth was most effective, treatment at 20 days of age was partially effective, and treatment in adulthood was ineffective. The effect of subsequent testosterone exposure in adulthood differed depending on the quality of the vocalization produced after E2 treatment alone. These results suggest that E2 may play a more important role than previously thought in the development of sex differences in vocal behavior. Furthermore, this study demonstrates that exogenous E2 treatment alone can induce vocal learning.
Age Factors↗
Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations.
Telencephalic nucleus HVC and its two efferent targets, RA and X, play essential roles in the production of complex, learned vocalizations in the male zebra finch. Normal females do not produce these learned vocalizations; HVC, RA, and X are small in volume, and HVC and RA are not synaptically connected. We have shown that estrogen treatment during development causes females to learn and produce male-like vocalizations. This article describes the neural masculinization of these E2 females, replicating and extending the work of others. Female zebra finches were treated with 17 beta-estradiol (E2) at hatching, at 14-22 days of age, or as adults. In adulthood, the volumes of nucleus RA and area X were measured and the efferent projections of nucleus HVC examined using the anterograde tracer PHA-L. Early, sustained E2 treatment caused the greatest increase in the volume of RA and X, the innervation of RA and X by HVC axons, and the masculinization of auditory responses of cells in RA. Treatments that lasted for a shorter period or started later in development resulted in different patterns of partial brain masculinization. E2 treatment in adulthood had no effect on the volume of RA or X or their innervation by HVC. Bilateral lesions of the tracheosyringeal nerves or of HVC had the same effects on the male-typical vocalizations produced by E2 females as they do on the vocalizations produced by males. These results demonstrate that the neural masculinization of telencephalic nuclei induced by E2 treatment sets up a functional circuit in females similar to one in males that enables the learning and production of complex vocalizations.
Age Factors↗
Neural mechanisms of vocal production in songbirds.
Recent reports have described peripheral and central mechanisms of vocal production in songbirds. Respiratory patterning, individual syringeal muscles and the two syringeal halves have been shown to make specific contributions to learned vocalizations. New information on the function and organization of central pathways suggests how these production mechanisms may be controlled. The results are opening new avenues for further work on how acquired motor patterns are represented in this system.
Animals↗
Brain pathways for learned and unlearned vocalizations differ in zebra finches.
Male zebra finches sing, females do not. However, both sexes produce the "long call" when placed in visual isolation. This call is sexually dimorphic; it includes learned components in males but not in females. The 3 learned features of the male long call are a high fundamental frequency, a fast frequency modulation, and a short, stable duration. These features are learned by the male during development, as is song. Since similar features are also found in song syllables, we wanted to know whether long-call production depends on the same CNS pathway that controls song production. Three critical components of the song pathway are telencephalic nuclei HVC, RA, and the tracheosyringeal (ts) nerves innervating the syrinx. In male zebra finches, bilateral section of the ts nerves affected the fundamental frequency and fast frequency modulations of both the long call and song but left the temporal features intact. Ts nerve section had no effect on the female long call. Bilateral lesions of either HVC or RA in males affected the fundamental frequency, fast frequency modulations, and temporal structure of both the long call and song. Similar lesions had no effect on the female long call. These results demonstrate that HVC, RA, and the ts nerves make critical contributions to the acoustic features of the male long call and song, while the temporal pattern depends on HVC and RA but not the ts nerves. HVC and RA lesions remove all the learned features that distinguish the male call and reveal a simple unlearned vocalization shared by both sexes. We suggest that the learned features of oscine songbird vocalizations are controlled by a telencephalic pathway that acts in concert with other pathways responsible for simpler, unlearned vocalizations.
Animals↗
Organization of the zebra finch song control system: I. Representation of syringeal muscles in the hypoglossal nucleus.
Understanding the representation of learned skills in the brain requires that one know the neural substrate for those skills. The avian song control system uses auditory information to establish and modify motor programs, which provide patterns for the excitation of individual muscles. In the present study, a combination of neurophysiological and anatomical techniques was used to map the representation of syringeal muscles in the tracheosyringeal part of the hypoglossal nucleus of adult male zebra finches. Microstimulation revealed that control zones for individual muscles are arranged along the rostrocaudal axis of the nucleus. The ventralis and dorsalis muscles have the largest domains, located at the rostral and caudal ends of the nucleus, respectively. The retrograde tracer fluorogold was applied to the muscles and confirmed this pattern. The muscle map obtained will provide a useful tool for further study of the convergence of muscle representation and sound representation in the more central portions of the song control pathway. This knowledge is essential for understanding how learned sounds are perceived and produced.
Animals↗