Songbirds provide a model for studying adult plasticity in the auditory cortex as a function of r... more Songbirds provide a model for studying adult plasticity in the auditory cortex as a function of recent experience due to its parallels with human auditory processing. As for human language, auditory processing in songbirds’ higher auditory cortex (caudomedial nidopallium, NCM) is lateralized for complex vocalization sounds. However, when Zebra finches are exposed to a novel heterospecific (canary) acoustic environment for a period of a few days, the typical pattern of right-lateralization is reversed. We now report that, in birds passively exposed to a novel heterospecific recording for extended periods (~21 days), the right-lateralized pattern of epidural auditory potentials reverses only transiently and then returns to the typical pattern. Using acute, bilateral multi-unit electrophysiology, we demonstrate that this dynamic pattern occurs in NCM. Furthermore, extended exposure enhances auditory discrimination for heterospecific stimuli. We conclude that lateralization is functiona...
1. Microstimulation (trains of biphasic current pulses at 50-400 Hz lasting 2-4 s) was delivered ... more 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.
The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 6, 2017
Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not... more Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not only on specific stimulus features, but also on previous experience that generates expectations about upcoming events. We studied the neural correlates of expectation in the songbird forebrain by using natural vocalizations as stimuli and manipulating the category and familiarity of context sounds. In our paradigm, we recorded bilaterally from auditory neurons in awake adult male zebra finches with multiple microelectrodes during repeated playback of a conspecific song, followed by further playback of this test song in different interleaved sequences with other conspecific or heterospecific songs. Significant enhancement in the auditory response to the test song was seen when its acoustic features differed from the statistical distribution of context song features, but not when it shared the same distribution. Enhancement was also seen when the time of occurrence of the test song was un...
Epigenetic mechanisms that modify chromatin conformation have recently been under investigation f... more Epigenetic mechanisms that modify chromatin conformation have recently been under investigation for their contributions to learning and the formation of memory. For example, the role of enzymes involved in histone acetylation are studied in the formation of long-lasting memories because memory consolidation requires gene expression events that are facilitated by an open state of chromatin. We recently proposed that epigenetic events may control the entry of specific sensory features into long-term memory by enabling transcription-mediated neuronal plasticity in sensory brain areas. Histone deacetylases, like HDAC3, may thereby regulate the specific sensory information that is captured for entry into long-term memory stores (Phan and Bieszczad, 2016). To test this hypothesis, we used an HDAC3-selective inhibitor (RGFP966) to determine whether its application after an experience with a sound stimulus with unique acoustic features could contribute to the formation of a memory that woul...
Sensory and motor brain structures work in collaboration during perception. To evaluate their res... more Sensory and motor brain structures work in collaboration during perception. To evaluate their respective contributions, the present study recorded neural responses to auditory stimulation at multiple sites simultaneously in both the higher-order auditory area NCM and the premotor area HVC of the songbird brain in awake zebra finches ( Taeniopygia guttata). Bird’s own song (BOS) and various conspecific songs (CON) were presented in both blocked and shuffled sequences. Neural responses showed plasticity in the form of stimulus-specific adaptation, with markedly different dynamics between the two structures. In NCM, the response decrease with repetition of each stimulus was gradual and long-lasting and did not differ between the stimuli or the stimulus presentation sequences. In contrast, HVC responses to CON stimuli decreased much more rapidly in the blocked than in the shuffled sequence. Furthermore, this decrease was more transient in HVC than in NCM, as shown by differential dynami...
How do social interactions form and modulate the neural representations of specific complex signa... more How do social interactions form and modulate the neural representations of specific complex signals? This question can be addressed in the songbird auditory system. Like humans, songbirds learn to vocalize by imitating tutors heard during development. These learned vocalizations are important in reproductive and social interactions and in individual recognition. As a model for the social reinforcement of particular songs, male zebra finches were trained to peck for a food reward in response to one song stimulus (GO) and to withhold responding for another (NoGO). After performance reached criterion, single and multiunit neural responses to both trained and novel stimuli were obtained from multiple electrodes inserted bilaterally into two songbird auditory processing areas [caudomedial mesopallium (CMM) and caudomedial nidopallium (NCM)] of awake, restrained birds. Neurons in these areas undergo stimulus-specific adaptation to repeated song stimuli, and responses to familiar stimuli a...
Projections from the telecephalic vocal control nucleus robustus archistriatalis (RA) to the brai... more 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.
Proceedings of the National Academy of Sciences, 1992
We investigated the participation of genomic regulatory events in the response of the songbird br... more 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 response...
Proceedings of the National Academy of Sciences, 1996
Auditory responses in the caudomedial neostriatum (NCM) of the zebra finch (Taeniopygia guttata) ... more 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 p...
its internalized gain function relating initial display derivatives to required force. 4. In expe... more its internalized gain function relating initial display derivatives to required force. 4. In experiments where feedback was delayed after giving a first target stimulus such that the compensatory display failed to reflect the animal's initial response, the animal emitted a new updated response 70-80 ms after the first. The display trajectory which caused the cat to update its response on delayed feedback trial was identical to that of control trials with long reaction times. In this case, however, the information eliciting response updating had to be derived as a difference between the actual display trajectory and that expected by the animal, based on its experience with the tracking task. This suggests that the animal develops an internal model of display properties which is used to determine when a new response is required.
Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to responses in o... more Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to 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 dep...
To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pu... more To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pure tone stimuli (250-5000 Hz) were recorded at 373 sites throughout the avian analogue of the mammalian auditory cortex in the caudal telencephalon of awake, restrained canaries. We found that a dorso-ventral tonotopic gradient from low to high frequency stimuli extends from the rostral field L2 to caudal-most caudo-medial nidopallium (NCM), similar to the frequency-dependent patterns of ZENK gene expression in canary NCM and to electrophysiological responses in other songbird species. However, response characteristics differ across the region. In field L2, responses are vigorous, phasic, and do not habituate to repeated presentations of the same stimulus. In an important subset of field L2 sites, tuning width narrows over the course of the response, which then terminates rapidly at stimulus offset. These properties are associated with inhibition at many nonpreferred frequencies and poststimulus inhibition at responsive frequencies. In contrast, NCM sites habituate to repeated sine waves, have wider tuning and lower amplitude responses, and rarely show inhibitory effects. Tuning curves in NCM are also flatter than those of field L2, and are often multipeaked. In addition, tuning width increases as the response unfolds and poststimulus excitation is often sustained in NCM. In sum, specific parts of the canary caudo-medial telencephalon differ in their response properties, suggesting differential roles in auditory processing. NCM properties, in particular, may allow for response integration across multiple spectrally varying stimulus elements, such as those that occur during birdsong.
Songbirds provide a model for studying adult plasticity in the auditory cortex as a function of r... more Songbirds provide a model for studying adult plasticity in the auditory cortex as a function of recent experience due to its parallels with human auditory processing. As for human language, auditory processing in songbirds’ higher auditory cortex (caudomedial nidopallium, NCM) is lateralized for complex vocalization sounds. However, when Zebra finches are exposed to a novel heterospecific (canary) acoustic environment for a period of a few days, the typical pattern of right-lateralization is reversed. We now report that, in birds passively exposed to a novel heterospecific recording for extended periods (~21 days), the right-lateralized pattern of epidural auditory potentials reverses only transiently and then returns to the typical pattern. Using acute, bilateral multi-unit electrophysiology, we demonstrate that this dynamic pattern occurs in NCM. Furthermore, extended exposure enhances auditory discrimination for heterospecific stimuli. We conclude that lateralization is functiona...
1. Microstimulation (trains of biphasic current pulses at 50-400 Hz lasting 2-4 s) was delivered ... more 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.
The Journal of neuroscience : the official journal of the Society for Neuroscience, Jan 6, 2017
Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not... more Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not only on specific stimulus features, but also on previous experience that generates expectations about upcoming events. We studied the neural correlates of expectation in the songbird forebrain by using natural vocalizations as stimuli and manipulating the category and familiarity of context sounds. In our paradigm, we recorded bilaterally from auditory neurons in awake adult male zebra finches with multiple microelectrodes during repeated playback of a conspecific song, followed by further playback of this test song in different interleaved sequences with other conspecific or heterospecific songs. Significant enhancement in the auditory response to the test song was seen when its acoustic features differed from the statistical distribution of context song features, but not when it shared the same distribution. Enhancement was also seen when the time of occurrence of the test song was un...
Epigenetic mechanisms that modify chromatin conformation have recently been under investigation f... more Epigenetic mechanisms that modify chromatin conformation have recently been under investigation for their contributions to learning and the formation of memory. For example, the role of enzymes involved in histone acetylation are studied in the formation of long-lasting memories because memory consolidation requires gene expression events that are facilitated by an open state of chromatin. We recently proposed that epigenetic events may control the entry of specific sensory features into long-term memory by enabling transcription-mediated neuronal plasticity in sensory brain areas. Histone deacetylases, like HDAC3, may thereby regulate the specific sensory information that is captured for entry into long-term memory stores (Phan and Bieszczad, 2016). To test this hypothesis, we used an HDAC3-selective inhibitor (RGFP966) to determine whether its application after an experience with a sound stimulus with unique acoustic features could contribute to the formation of a memory that woul...
Sensory and motor brain structures work in collaboration during perception. To evaluate their res... more Sensory and motor brain structures work in collaboration during perception. To evaluate their respective contributions, the present study recorded neural responses to auditory stimulation at multiple sites simultaneously in both the higher-order auditory area NCM and the premotor area HVC of the songbird brain in awake zebra finches ( Taeniopygia guttata). Bird’s own song (BOS) and various conspecific songs (CON) were presented in both blocked and shuffled sequences. Neural responses showed plasticity in the form of stimulus-specific adaptation, with markedly different dynamics between the two structures. In NCM, the response decrease with repetition of each stimulus was gradual and long-lasting and did not differ between the stimuli or the stimulus presentation sequences. In contrast, HVC responses to CON stimuli decreased much more rapidly in the blocked than in the shuffled sequence. Furthermore, this decrease was more transient in HVC than in NCM, as shown by differential dynami...
How do social interactions form and modulate the neural representations of specific complex signa... more How do social interactions form and modulate the neural representations of specific complex signals? This question can be addressed in the songbird auditory system. Like humans, songbirds learn to vocalize by imitating tutors heard during development. These learned vocalizations are important in reproductive and social interactions and in individual recognition. As a model for the social reinforcement of particular songs, male zebra finches were trained to peck for a food reward in response to one song stimulus (GO) and to withhold responding for another (NoGO). After performance reached criterion, single and multiunit neural responses to both trained and novel stimuli were obtained from multiple electrodes inserted bilaterally into two songbird auditory processing areas [caudomedial mesopallium (CMM) and caudomedial nidopallium (NCM)] of awake, restrained birds. Neurons in these areas undergo stimulus-specific adaptation to repeated song stimuli, and responses to familiar stimuli a...
Projections from the telecephalic vocal control nucleus robustus archistriatalis (RA) to the brai... more 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.
Proceedings of the National Academy of Sciences, 1992
We investigated the participation of genomic regulatory events in the response of the songbird br... more 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 response...
Proceedings of the National Academy of Sciences, 1996
Auditory responses in the caudomedial neostriatum (NCM) of the zebra finch (Taeniopygia guttata) ... more 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 p...
its internalized gain function relating initial display derivatives to required force. 4. In expe... more its internalized gain function relating initial display derivatives to required force. 4. In experiments where feedback was delayed after giving a first target stimulus such that the compensatory display failed to reflect the animal's initial response, the animal emitted a new updated response 70-80 ms after the first. The display trajectory which caused the cat to update its response on delayed feedback trial was identical to that of control trials with long reaction times. In this case, however, the information eliciting response updating had to be derived as a difference between the actual display trajectory and that expected by the animal, based on its experience with the tracking task. This suggests that the animal develops an internal model of display properties which is used to determine when a new response is required.
Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to responses in o... more Neurons in nuclei on the motor pathway for vocalizations in songbirds are known to 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 dep...
To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pu... more To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pure tone stimuli (250-5000 Hz) were recorded at 373 sites throughout the avian analogue of the mammalian auditory cortex in the caudal telencephalon of awake, restrained canaries. We found that a dorso-ventral tonotopic gradient from low to high frequency stimuli extends from the rostral field L2 to caudal-most caudo-medial nidopallium (NCM), similar to the frequency-dependent patterns of ZENK gene expression in canary NCM and to electrophysiological responses in other songbird species. However, response characteristics differ across the region. In field L2, responses are vigorous, phasic, and do not habituate to repeated presentations of the same stimulus. In an important subset of field L2 sites, tuning width narrows over the course of the response, which then terminates rapidly at stimulus offset. These properties are associated with inhibition at many nonpreferred frequencies and poststimulus inhibition at responsive frequencies. In contrast, NCM sites habituate to repeated sine waves, have wider tuning and lower amplitude responses, and rarely show inhibitory effects. Tuning curves in NCM are also flatter than those of field L2, and are often multipeaked. In addition, tuning width increases as the response unfolds and poststimulus excitation is often sustained in NCM. In sum, specific parts of the canary caudo-medial telencephalon differ in their response properties, suggesting differential roles in auditory processing. NCM properties, in particular, may allow for response integration across multiple spectrally varying stimulus elements, such as those that occur during birdsong.
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Papers by David VICARIO