Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure.

Sensitivity to the sequential structure of communication sounds is fundamental not only for language comprehension in humans but also for song recognition in songbirds. By quantifying single-unit responses, we first assessed whether the sequential order of song elements, called syllables, in conspecific songs is encoded in a secondary auditory cortex-like region of the zebra finch brain. Based on a habituation/dishabituation paradigm, we show that, after multiple repetitions of the same conspecific song, rearranging syllable order reinstated strong responses. A large proportion of neurons showed sensitivity to song context in which syllables occurred providing support for the nonlinear processing of syllable sequences. Sensitivity to the temporal order of items within a sequence should enable learning its underlying structure, an ability considered a core mechanism of the human language faculty. We show that repetitions of songs that were ordered according to a specific grammatical structure (i.e., ABAB or AABB structures; A and B denoting song syllables) led to different responses in both anesthetized and awake birds. Once responses were decreased due to song repetitions, the transition from one structure to the other could affect the firing rates and/or the spike patterns. Our results suggest that detection was based on local differences rather than encoding of the global song structure as a whole. Our study demonstrates that a high-level auditory region provides neuronal mechanisms to help discriminate stimuli that differ in their sequential structure.SIGNIFICANCE STATEMENT Sequence processing has been proposed as a potential precursor of language syntax. As a sequencing operation, the encoding of the temporal order of items within a sequence may help in recognition of relationships between adjacent items and in learning the underlying structure. Taking advantage of the stimulus-specific adaptation phenomenon observed in a high-level auditory region of the zebra finch brain, we addressed this question at the neuronal level. Reordering elements within conspecific songs reinstated robust responses. Neurons also detected changes in the structure of artificial songs, and this detection depended on local transitions between adjacent or nonadjacent syllables. These findings establish the songbird as a model system for deciphering the mechanisms underlying sequence processing at the single-cell level.

Multisensory processes in birds: From single neurons to the influence of social interactions and sensory loss.

World experiences involve multisensory stimulation that arises simultaneously from multiple sources. Yet, we experience a coherent and unified world. Many studies have focused on how sensory information from distinct modalities are integrated and showed that numerous behavioural and cognitive benefits are provided by multisensory processes. Much work has been done with mammalian models but research on avian species also expands our knowledge on multisensory processes. Avian species exhibit a great diversity of behaviours and these species have provided evidence that multisensory processes benefit by the learning that occurs in natural situations. Cross-modal influences on the control of sensorimotor processes occur in circumstances of sensory loss. Also, studies suggest pervasive multisensory influences throughout the avian brain. This review summarizes research done on the imprinting behaviour of precocial bird species, on the ability of barn owls to detect prey and on the vocal communication of songbirds.

Distinct timescales for the neuronal encoding of vocal signals in a high-order auditory area.

The ability of the auditory system to selectively recognize natural sound categories while maintaining a certain degree of tolerance towards variations within these categories, which may have functional roles, is thought to be crucial for vocal communication. To date, it is still largely unknown how the balance between tolerance and sensitivity to variations in acoustic signals is coded at a neuronal level. Here, we investigate whether neurons in a high-order auditory area in zebra finches, a songbird species, are sensitive to natural variations in vocal signals by recording their responses to repeated exposures to identical and variant sound sequences. We used the songs of male birds which tend to be highly repetitive with only subtle variations between renditions. When playing these songs to both anesthetized and awake birds, we found that variations between songs did not affect the neuron firing rate but the temporal reliability of responses. This suggests that auditory processing operates on a range of distinct timescales, namely a short one to detect variations in vocal signals, and longer ones that allow the birds to tolerate variations in vocal signal structure and to encode the global context.

Influence of social conditions in song sharing in the adult canary.

In songbirds, experience of social and environmental cues during a discrete period after birth may dramatically influence song learning. In the canary, the ability to learn new songs is assumed to persist throughout life. The aim of the present study was to investigate whether social context could guide changes in adult song. Three groups of canaries were kept in different social and temporal conditions. Results showed that the multiple hierarchical levels of the canary song structure were affected by social environment: songs of males housed together for 2 years were more similar than those of males that spent the same time in individual cages in regard to acoustic parameters, syllable repertoire and repertoire of sequences of two-syllable types. However, social housing did not result in the emergence of a group-specific vocal signature within songs. In conclusion, these results suggested that under the influence of social factors, a copying process could allow adult canaries to adjust, at least in part, their songs to those of other individuals.

Neural mechanisms of vocal imitation: The role of sleep replay in shaping mirror neurons.

Learning by imitation involves not only perceiving another individual's action to copy it, but also the formation of a memory trace in order to gradually establish a correspondence between the sensory and motor codes, which represent this action through sensorimotor experience. Memory and sensorimotor processes are closely intertwined. Mirror neurons, which fire both when the same action is performed or perceived, have received considerable attention in the context of imitation. An influential view of memory processes considers that the consolidation of newly acquired information or skills involves an active offline reprocessing of memories during sleep within the neuronal networks that were initially used for encoding. Here, we review the recent advances in the field of mirror neurons and offline processes in the songbird. We further propose a theoretical framework that could establish the neurobiological foundations of sensorimotor learning by imitation. We propose that the reactivation of neuronal assemblies during offline periods contributes to the integration of sensory feedback information and the establishment of sensorimotor mirroring activity at the neuronal level.

Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia-forebrain circuit.

The plasticity of nervous systems allows animals to quickly adapt to a changing environment. In particular, seasonal plasticity of brain structure and behavior is often critical to survival or mating in seasonal climates. Songbirds provide striking examples of seasonal changes in neural circuits and vocal behavior and have emerged as a leading model for adult brain plasticity. While seasonal plasticity and the well-characterized process of juvenile song learning may share common neural mechanisms, the extent of their similarity remains unclear. Especially, it is unknown whether the basal ganglia (BG)-forebrain loop which implements song learning in juveniles by driving vocal exploration participates in seasonal plasticity. To address this issue, we performed bilateral lesions of the output structure of the song-related BG-forebrain circuit (the magnocellular nucleus of the anterior nidopallium) in canaries during the breeding season, when song is most stereotyped, and just after resuming singing in early fall, when canaries sing their most variable songs and may produce new syllable types. Lesions drastically reduced song acoustic variability, increased song and phrase duration, and decreased syntax variability in early fall, reverting at least partially seasonal changes observed between the breeding season and early fall. On the contrary, lesions did not affect singing behavior during the breeding season. Our results therefore indicate that the BG-forebrain pathway introduces acoustic and syntactic variability in song when canaries resume singing in early fall. We propose that BG-forebrain circuits actively participate in seasonal plasticity by injecting variability in behavior during non-breeding season. SIGNIFICANCE STATEMENT: The study of seasonal plasticity in temperate songbirds has provided important insights into the mechanisms of structural and functional plasticity in the central nervous system. The precise function and mechanisms of seasonal song plasticity however remain poorly understood. We show here that a basal ganglia-forebrain circuit involved in the acquisition and maintenance of birdsong is actively inducing song variability outside the breeding season, when singing is most variable, while having little effect on the stereotyped singing during the breeding season. Our results suggest that seasonal plasticity reflects an active song-maintenance process akin to juvenile learning, and that basal ganglia-forebrain circuits can drive plasticity in a learned vocal behavior during the non-injury-induced degeneration and reconstruction of the neural circuit underlying its production.

Selectivity of canary HVC neurons for the bird's own song: modulation by photoperiodic conditions.

To what extent seasonal factors modify the neuronal functional properties within the nuclei of the avian song system remains an open question. In adult songbirds, neurons of the song premotor nucleus HVC (used as a proper name) exhibit selective responses for the bird's own song (BOS). Here we examine whether, outside the breeding season, when songs are less stereotyped, HVC neurons of male canaries still respond selectively to the BOS produced during this period. In an initial experiment, single-unit recordings (n = 114) revealed that the neuronal selectivity for the current BOS was attenuated in males exposed to a short-day photoperiod (typical of the nonbreeding season) compared with that found in males exposed to a long-day photoperiod. In long-day conditions, 35% of the cells responded to the BOS, whereas only 12% did in short-day conditions; there were four times more selective cells (d' > 1) in long-day than in short-day conditions. To determine whether these effects were the consequence of differences in acoustic features between breeding and nonbreeding songs, neurons (n = 72) recorded in short-day conditions were tested with both a short-day BOS and a long-day BOS. A low percentage of neurons exhibited responses to short-day or to long-day BOS (11% for each song). Responses of putative interneurons (spike duration < 0.4 ms) and of putative relay cells were similarly attenuated by the short-day conditions. These results strongly suggest that, in canary, rather than being a fixed property, the selectivity for the BOS moves along a continuum and peaks when the day length mimics the breeding conditions.

Sex differences in the representation of call stimuli in a songbird secondary auditory area.

Understanding how communication sounds are encoded in the central auditory system is critical to deciphering the neural bases of acoustic communication. Songbirds use learned or unlearned vocalizations in a variety of social interactions. They have telencephalic auditory areas specialized for processing natural sounds and considered as playing a critical role in the discrimination of behaviorally relevant vocal sounds. The zebra finch, a highly social songbird species, forms lifelong pair bonds. Only male zebra finches sing. However, both sexes produce the distance call when placed in visual isolation. This call is sexually dimorphic, is learned only in males and provides support for individual recognition in both sexes. Here, we assessed whether auditory processing of distance calls differs between paired males and females by recording spiking activity in a secondary auditory area, the caudolateral mesopallium (CLM), while presenting the distance calls of a variety of individuals, including the bird itself, the mate, familiar and unfamiliar males and females. In males, the CLM is potentially involved in auditory feedback processing important for vocal learning. Based on both the analyses of spike rates and temporal aspects of discharges, our results clearly indicate that call-evoked responses of CLM neurons are sexually dimorphic, being stronger, lasting longer, and conveying more information about calls in males than in females. In addition, how auditory responses vary among call types differ between sexes. In females, response strength differs between familiar male and female calls. In males, temporal features of responses reveal a sensitivity to the bird's own call. These findings provide evidence that sexual dimorphism occurs in higher-order processing areas within the auditory system. They suggest a sexual dimorphism in the function of the CLM, contributing to transmit information about the self-generated calls in males and to storage of information about the bird's auditory experience in females.

Sex and season influence the proportion of thin spike cells in the canary HVc.

In songbirds, anatomical attributes of song nuclei exhibit sexual and seasonal differences. To extend these data to physiological correlates, neurons ( n= 374) were recorded in the HVc of male and female canaries during and outside the breeding period. Surprisingly, a particular type of action potential waveforms was observed more frequently in breeding than in non-breeding birds and in males than in females. These neurons showed both a shorter action potential duration (< 0.4 ms) and a higher firing rate (2.5 1.4 spikes/s) than the other neurons. Such characteristics are usually associated with interneurons in the songbird HVc as well as in the mammalian neocortex. Thus, these results provide the first electrophysiological evidence for an alteration of the neuronal network of HVc across sexes and seasons.

The selectivity of canary HVC neurons for the Bird's Own Song: rate coding, temporal coding, or both?

The neuronal selectivity observed in the avian song system for the Bird's Own Song progressively emerged as an extraordinary fruitful model to investigate the neural code underlying the recognition of complex stimuli and the occurrence of learned behaviors. In adult zebra finch, neurons from the HVC (used as a proper name) show very selective auditory responses, firing more to presentation of the Bird's Own Song (BOS) than to reverse BOS or other conspecific songs. However, as adult zebra finches always produce the same stereotyped song, the presence of such highly selective neurons in birds with larger repertoire still remains an open question. Data presented here show that neurons selective for the BOS can be found in adult canary, a seasonal breeding bird which display a large repertoire. More precisely, we found that a large proportion of neurons (29/36) exhibits higher responses to presentation of the forward than to the reverse BOS, and that 22% of the cells were identified as selective on the basis of the d' value. For a cell that was extensively studied, we evaluated to what extent temporal stimulus-related structure predicts the acoustic stimulus using linear or non-linear artificial neural networks (ANN). These analyses indicated that the temporal structure contained in spike trains characterizes more accurately the stimulus than the firing rate. The limitations of applying ANN analyses to electrophysiological data are discussed and potential solutions to increase the confidence in these analysis are proposed.

Noradrenergic control of auditory information processing in female canaries.

An ethological procedure, based on the study of the sexual responsiveness of female canaries (Serinus canaria) to song playbacks was used to investigate the function of central noradrenergic inputs in the processing of auditory information. The effects of a noradrenergic denervation on sexual responses was analyzed in females exposed to playbacks of biological relevant auditory stimuli, i.e. sexually stimulating songs, presented alone or masked by auditory distractors. A decrease in behavioral responsiveness was observed as a function of the amount of masking distractors indicating that female canaries have the perceptual ability to discriminate and selectively attend to biologically relevant songs. After the systemic administration of DSP-4, a specific noradrenergic neurotoxin, females exhibited an overall decrease in sexual responsiveness to songs masked or not by distractors. No effect of DSP-4 were detected on the motor activity nor on reproductive behaviors. These results indicate that central noradrenergic inputs modulate the sexual behavior of female canaries by affecting the auditory processing of relevant information contained in sexually stimulating songs.

A species-specific view of song representation in a sensorimotor nucleus.

Songbirds constitute a powerful model system for the investigation of how complex vocal communication sounds are represented and generated, offering a neural system in which the brain areas involved in auditory, motor and auditory-motor integration are well known. One brain area of considerable interest is the nucleus HVC. Neurons in the HVC respond vigorously to the presentation of the bird's own song and display song-related motor activity. In the present paper, we present a synthesis of neurophysiological studies performed in the HVC of one songbird species, the canary (Serinus canaria). These studies, by taking advantage of the singing behavior and song characteristics of the canary, have examined the neuronal representation of the bird's own song in the HVC. They suggest that breeding cues influence the degree of auditory selectivity of HVC neurons for the bird's own song over its time-reversed version, without affecting the contribution of spike timing to the information carried by these two song stimuli. Also, while HVC neurons are collectively more responsive to forward playback of the bird's own song than to its temporally or spectrally modified versions, some are more broadly tuned, with an auditory responsiveness that extends beyond the bird's own song. Lastly, because the HVC is also involved in song production, we discuss the peripheral control of song production, and suggest that interspecific variations in song production mechanisms could be exploited to improve our understanding of the functional role of the HVC in respiratory-vocal coordination.

Repertoire sharing and auditory responses in the HVC of the canary.

In songbirds, auditory neurons of the nucleus HVC respond selectively to a particular complex sound, the bird's own song (BOS). In the canary, this song selectivity did not exclude responses to conspecific songs. Here, we recorded single units in nucleus HVC of adult canaries to assess to what extent repertoire sharing among birds contributed to auditory responsiveness to birds' songs other than the BOS. Results indicated that song phrases driving auditory responses could differ from bird's own phrases suggesting that a subset of neurons were not strictly tuned to acoustic features of self-generated song components. In the canary, auditory representation of the BOSs might be more complex than that which has been described for birds with a small repertoire.

Contribution of spike timing to the information transmitted by HVC neurons.

In many species, neurons with highly selective stimulus-response properties characterize higher order sensory areas and/or sensory motor areas of the CNS. In the songbird nuclei, the responses of HVC (used as a proper name) neurons during playback of the bird's own song (BOS) are probably one of the most striking examples of selectivity for natural stimuli. We examined here to what extent spike-timing carries information about natural and time-reversed versions of the BOS. From a heterogenous population of 107 HVC neurons recorded in long-day or short-day conditions, a standard indicator of stimulus preference based on spike-count (the d' index) indicates that a limited proportion of cells can be classified as selective for the BOS (20% with a |d'| > 1). In contrast, quantifying the information conveyed by spike trains with the metric-space of J.D. Victor & K.P Purpura [(1996) J. Neurophysiol., 76, 1310-1326] indicates that 62% of the cells display significant amounts of transmitted information, among which 77% are 'temporal cells'. 'Temporal cells' correspond to cells transmitting significant amounts of information when spike-timing is considered, whereas no information, or lower amounts of transmitted information, is obtained when only spike-count is considered. Computing a correlation index between spike trains [S. Schreiber et al. (2003) Neurocomputing, 52-54,925-931] revealed that spike-timing reliability is higher for the forward than for the reverse BOS, whatever the day length and the cell type are. Cells classified as selective in terms of spike-counts (d' index) had greater amounts of transmitted information, but cells classified as non-selective (d' < 0.5) can also transmit significant amounts of information. Thus, information theory methods demonstrate that a much larger proportion of neurons than expected based on spike-count only participate in the discrimination between stimuli.