Novel sound exposure drives dynamic changes in auditory lateralization that are associated with perceptual learning in zebra finches.

Songbirds provide a model for adult plasticity in the auditory cortex as a function of recent experience due to parallels with human auditory processing. As for speech processing in humans, activity in songbirds' higher auditory cortex (caudomedial nidopallium, NCM) is lateralized for complex vocalization sounds. However, in Zebra finches exposed to a novel heterospecific (canary) acoustic environment for 4-9 days, the typical pattern of right-lateralization is reversed.

Dynamic encoding of phonetic categories in zebra finch auditory forebrain.

Vocal communication requires the formation of acoustic categories to enable invariant representations of sounds despite superficial variations. Humans form acoustic categories for speech phonemes, enabling the listener to recognize words independent of speakers; animals can also discriminate speech phonemes. We investigated the neural mechanisms of this process using electrophysiological recordings from the zebra finch secondary auditory area, caudomedial nidopallium (NCM), during passive exposure to human speech stimuli consisting of two naturally spoken words produced by multiple speakers.

Statistical learning of transition patterns in the songbird auditory forebrain.

Statistical learning of transition patterns between sounds-a striking capability of the auditory system-plays an essential role in animals' survival (e.g., detect deviant sounds that signal danger).

Rapid and long-lasting improvements in neural discrimination of acoustic signals with passive familiarization.

Sensory representations in the adult brain must undergo dynamic changes to adapt to the complexity of the external world. This study investigated how passive exposure to novel sounds modifies neural representations to facilitate recognition and discrimination, using the zebra finch model organism. The neural responses in an auditory structure in the zebra finch brain, Caudal Medial Nidopallium (NCM), undergo a long-term form of adaptation with repeated stimulus presentation, providing an excellent substrate to probe the neural underpinnings of adaptive sensory representations.

Neural Correlate of Transition Violation and Deviance Detection in the Songbird Auditory Forebrain.

Deviants are stimuli that violate one's prediction about the incoming stimuli. Studying deviance detection helps us understand how nervous system learns temporal patterns between stimuli and forms prediction about the future. Detecting deviant stimuli is also critical for animals' survival in the natural environment filled with complex sounds and patterns.

Familiar But Unexpected: Effects of Sound Context Statistics on Auditory Responses in the Songbird Forebrain.

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.

HDAC3 Inhibitor RGFP966 Modulates Neuronal Memory for Vocal Communication Signals in a Songbird Model.

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.

Principles of auditory processing differ between sensory and premotor structures of the songbird forebrain.

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 (). Bird's own song (BOS) and various conspecific songs (CON) were presented in both blocked and shuffled sequences.

Neural responses in songbird forebrain reflect learning rates, acquired salience, and stimulus novelty after auditory discrimination training.

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.

Hemispheric asymmetry in new neurons in adulthood is associated with vocal learning and auditory memory.

Many brain regions exhibit lateral differences in structure and function, and also incorporate new neurons in adulthood, thought to function in learning and in the formation of new memories. However, the contribution of new neurons to hemispheric differences in processing is unknown. The present study combines cellular, behavioral, and physiological methods to address whether 1) new neuron incorporation differs between the brain hemispheres, and 2) the degree to which hemispheric lateralization of new neurons correlates with behavioral and physiological measures of learning and memory.

Statistical learning of recurring sound patterns encodes auditory objects in songbird forebrain.

Auditory neurophysiology has demonstrated how basic acoustic features are mapped in the brain, but it is still not clear how multiple sound components are integrated over time and recognized as an object. We investigated the role of statistical learning in encoding the sequential features of complex sounds by recording neuronal responses bilaterally in the auditory forebrain of awake songbirds that were passively exposed to long sound streams. These streams contained sequential regularities, and were similar to streams used in human infants to demonstrate statistical learning for speech sounds.

He hears, she hears: are there sex differences in auditory processing?

Songbirds learn individually unique songs through vocal imitation and use them in courtship and territorial displays. Previous work has identified a forebrain auditory area, the caudomedial nidopallium (NCM), that appears specialized for discriminating and remembering conspecific vocalizations. In zebra finches (ZFs), only males produce learned vocalizations, but both sexes process these and other signals.

Blocking estradiol synthesis affects memory for songs in auditory forebrain of male zebra finches.

Estradiol (E2) has recently been shown to modulate sensory processing in an auditory area of the songbird forebrain, the caudomedial nidopallium (NCM). When a bird hears conspecific song, E2 increases locally in NCM, where neurons express both the aromatase enzyme that synthesizes E2 from precursors and estrogen receptors. Auditory responses in NCM show a form of neuronal memory: repeated playback of the unique learned vocalizations of conspecific individuals induces long-lasting stimulus-specific adaptation of neural responses to each vocalization.

To modulate and be modulated: estrogenic influences on auditory processing of communication signals within a socio-neuro-endocrine framework.

Gonadal hormones modulate behavioral responses to sexual stimuli, and communication signals can also modulate circulating hormone levels. In several species, these combined effects appear to underlie a two-way interaction between circulating gonadal hormones and behavioral responses to socially salient stimuli. Recent work in songbirds has shown that manipulating local estradiol levels in the auditory forebrain produces physiological changes that affect discrimination of conspecific vocalizations and can affect behavior.

Hemispheric differences in processing of vocalizations depend on early experience.

An intriguing phenomenon in the neurobiology of language is lateralization: the dominant role of one hemisphere in a particular function. Lateralization is not exclusive to language because lateral differences are observed in other sensory modalities, behaviors, and animal species. Despite much scientific attention, the function of lateralization, its possible dependence on experience, and the functional implications of such dependence have yet to be clearly determined.

Response properties of the auditory telencephalon in songbirds change with recent experience and season.

The caudomedial nidopallium (NCM) is a telencephalic auditory area that is selectively activated by conspecific vocalizations in zebra finches and canaries. We recently demonstrated that temporal and spectral dynamics of auditory tuning in NCM differ between these species [1]. In order to determine whether these differences reflect recent experience, we exposed separate groups of each species and sex to different housing conditions.

Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong.

Species differences in auditory processing dynamics in songbird auditory telencephalon.

The caudomedial nidopallium (NCM) of songbirds is a telencephalic area involved in the auditory processing and memorization of complex vocal communication signals. We used pure tone stimuli and multiunit electrophysiological recordings in awake birds to investigate whether the basic properties of song-responding circuits in NCM differ between canaries and zebra finches, two species whose songs are markedly different in their spectral and temporal organization. We found that the responses in zebra finch NCM are characterized by broad tuning and sustained responses that may facilitate the integration of zebra finch song syllables and call notes that are of long duration and have a broad harmonic structure.

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.

Auditory topography and temporal response dynamics of canary caudal telencephalon.

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.

Using learned calls to study sensory-motor integration in songbirds.

Communicating songbirds produce calls as well as song and some of these are learned. One of these-the long call in zebra finches-is used by both sexes in similar behavioral contexts, but is learned in males and not in females. The male long call includes learned spectral and temporal features.