Transformation of temporal sequences in the zebra finch auditory system.
Ontology highlight
ABSTRACT:
SUBMITTER: Lim Y
PROVIDER: S-EPMC5161447 | biostudies-literature | 2016 Nov
REPOSITORIES: biostudies-literature
Publications
Transformation of temporal sequences in the zebra finch auditory system.
Lim Yoonseob Y Lagoy Ryan R Shinn-Cunningham Barbara G BG Gardner Timothy J TJ
eLife 20161129
This study examines how temporally patterned stimuli are transformed as they propagate from primary to secondary zones in the thalamorecipient auditory pallium in zebra finches. Using a new class of synthetic click stimuli, we find a robust mapping from temporal sequences in the primary zone to distinct population vectors in secondary auditory areas. We tested whether songbirds could discriminate synthetic click sequences in an operant setup and found that a robust behavioral discrimination is p ...[more]
Similar Datasets
Project description:Despite being commonly referenced throughout neuroscientific research on songbirds, reports of hemispheric specialization in the processing of song remain controversial. The notion of such asymmetries in songbirds is further complicated by evidence that both cerebral hemispheres in humans may be specialized for different aspects of speech perception. Some studies suggest that the auditory neural substrates in the left and right hemispheres of humans process temporal and spectral elements within speech sounds, respectively. To determine whether songbirds process their conspecific songs in such a complementary, bilateral manner, we performed functional magnetic resonance imaging (fMRI) on 15 isoflurane anesthetized adult male zebra finches (Taeniopygia guttata) while presenting them with (1) non-manipulated, (2) spectrally-filtered (reduced spectral structure), and (3) temporally-filtered (reduced temporal structure) conspecific song. Our results revealed sensitivity of both primary (Field L) and secondary (caudomedial nidopallium, NCM) auditory regions to changes in spectral and temporal structure of song. On the one hand, temporally-filtered song elicited a bilateral decrease in neural responses compared to the other stimulus types. On the other hand, spectrally filtered song elicited significantly greater responses in left Field L and NCM than temporally filtered or non-manipulated song while concurrently reducing the response relative to non-manipulated song in the right auditory forebrain. The latter hemispheric difference in sensitivity to manipulations of spectral structure in song, suggests that there is an asymmetry in spectral and temporal domain processing in the zebra finch auditory forebrain bearing some resemblance to what has been observed in human auditory cortex.
| S-EPMC5633600 | biostudies-literature
Project description:Songbirds learn to sing much as humans learn to speak. In zebra finches, one of the premier songbird models, males learn to sing for later courtship through a multistep learning process during the developmental period. They first listen to and memorize the song of a tutor (normally their father) during the sensory learning period. Then, in the subsequent sensory-motor learning phase (with large overlap), they match their vocalizations to the memorized tutor song via auditory feedback and develop their own unique songs, which they maintain throughout their lives. Previous studies have suggested that memories of tutor songs are shaped in the caudomedial nidopallium (NCM) of the brain, which is analogous to the mammalian higher auditory cortex. Isolation during development, which extends the sensory learning period in males, alters song preference in adult females, and NCM inactivation decreases song preference. However, the development of neurophysiological properties of neurons in this area and the effect of isolation on these neurons have not yet been explained. Here, we performed whole-cell patch-clamp recording on NCM neurons from juvenile zebra finches during the sensory learning period, 20, 40, or 60 days post-hatching (DPH) and examined their neurophysiological properties. In contrast to previous reports in adult NCM neurons, the majority of NCM neurons of juvenile zebra finches showed spontaneous firing with or without burst firing patterns, and the percentage of neurons that fired increased in the middle of the sensory learning period (40 DPH) and then decreased at the end (60 DPH) in both males and females. We further found that auditory isolation from tutor songs alters developmental changes in the proportions of firing neurons both in males and females, and also changes those of burst neurons differently between males that sing and females that do not. Taken together, these findings suggest that NCM neurons develop their neurophysiological properties depending on auditory experiences during the sensory song learning period, which underlies memory formation for song learning in males and song discrimination in females.
| S-EPMC7578418 | biostudies-literature
Project description:In an important model for neuroscience, songbirds learn to discriminate songs they hear during tape-recorded playbacks, as demonstrated by song-specific habituation of both behavioral and neurogenomic responses in the auditory forebrain. We hypothesized that microRNAs (miRNAs or miRs) may participate in the changing pattern of gene expression induced by song exposure. To test this, we used massively parallel Illumina sequencing to analyse small RNAs from auditory forebrain of adult zebra finches exposed to tape-recorded birdsong or silence.In the auditory forebrain, we identified 121 known miRNAs conserved in other vertebrates. We also identified 34 novel miRNAs that do not align to human or chicken genomes. Five conserved miRNAs showed significant and consistent changes in copy number after song exposure across three biological replications of the song-silence comparison, with two increasing (tgu-miR-25, tgu-miR-192) and three decreasing (tgu-miR-92, tgu-miR-124, tgu-miR-129-5p). We also detected a locus on the Z sex chromosome that produces three different novel miRNAs, with supporting evidence from Northern blot and TaqMan qPCR assays for differential expression in males and females and in response to song playbacks. One of these, tgu-miR-2954-3p, is predicted (by TargetScan) to regulate eight song-responsive mRNAs that all have functions in cellular proliferation and neuronal differentiation.The experience of hearing another bird singing alters the profile of miRNAs in the auditory forebrain of zebra finches. The response involves both known conserved miRNAs and novel miRNAs described so far only in the zebra finch, including a novel sex-linked, song-responsive miRNA. These results indicate that miRNAs are likely to contribute to the unique behavioural biology of learned song communication in songbirds.
| S-EPMC3118218 | biostudies-literature
Project description:In birds the auditory system plays a key role in providing the sensory input used to discriminate between conspecific and heterospecific vocal signals. In those species that are known to learn their vocalizations, for example, songbirds, it is generally considered that this ability arises and is manifest in the forebrain, although there is no a priori reason why brainstem components of the auditory system could not also play an important part. To test this assumption, we used groups of normal reared and cross-fostered zebra finches that had previously been shown in behavioural experiments to reduce their preference for conspecific songs subsequent to cross fostering experience with Bengalese finches, a related species with a distinctly different song. The question we asked, therefore, is whether this experiential change also changes the bias in favour of conspecific song displayed by auditory midbrain units of normally raised zebra finches. By recording the responses of single units in MLd to a variety of zebra finch and Bengalese finch songs in both normally reared and cross-fostered zebra finches, we provide a positive answer to this question. That is, the difference in response to conspecific and heterospecific songs seen in normal reared zebra finches is reduced following cross-fostering. In birds the virtual absence of mammalian-like cortical projections upon auditory brainstem nuclei argues against the interpretation that MLd units change, as observed in the present experiments, as a result of top-down influences on sensory processing. Instead, it appears that MLd units can be influenced significantly by sensory inputs arising directly from a change in auditory experience during development.
| S-EPMC7384439 | biostudies-literature
Project description:The zebra finch brain features a set of clearly defined and hierarchically arranged motor nuclei that are selectively responsible for producing singing behavior. One of these regions, a critical forebrain structure called HVC, contains premotor neurons that are active at precise time points during song production. However, the neural representation of this behavior at a population level remains elusive. We used two-photon microscopy to monitor ensemble activity during singing, integrating across multiple trials by adopting a Bayesian inference approach to more precisely estimate burst timing. Additionally, we examined spiking and motor-related synaptic inputs using intracellular recordings during singing. With both experimental approaches, we find that premotor events do not occur preferentially at the onsets or offsets of song syllables or at specific subsyllabic motor landmarks. These results strongly support the notion that HVC projection neurons collectively exhibit a temporal sequence during singing that is uncoupled from ongoing movements.
| S-EPMC4941616 | biostudies-literature
Project description:Unlearned calls are produced by all birds whereas learned songs are only found in three avian taxa, most notably in songbirds. The neural basis for song learning and production is formed by interconnected song nuclei: the song control system. In addition to song, zebra finches produce large numbers of soft, unlearned calls, among which "stack" calls are uttered frequently. To determine unequivocally the calls produced by each member of a group, we mounted miniature wireless microphones on each zebra finch. We find that group living paired males and females communicate using bilateral stack calling. To investigate the role of the song control system in call-based male female communication, we recorded the electrical activity in a premotor nucleus of the song control system in freely behaving male birds. The unique combination of acoustic monitoring together with wireless brain recording of individual zebra finches in groups shows that the neuronal activity of the song system correlates with the production of unlearned stack calls. The results suggest that the song system evolved from a brain circuit controlling simple unlearned calls to a system capable of producing acoustically rich, learned vocalizations.
| S-EPMC4196903 | biostudies-literature
Project description:Like human speech, birdsong is a complex vocal behavior that is acquired by sensorimotor learning based on coordination of auditory input and vocal output to mimic memorized tutor song. Here we investigate neural circuits for vocal learning and production in deafened songbirds to elucidate how sensory-input regulate genetic and epigenetic property of vocal development and its associated gene expression dynamics. Compared with audition-intact birds, in deafened zebra finches, the vocal development is delayed but song crystallization is observed at more than three times later, producing individually different but structured vocal patterns. In contrast to the distinct difference of vocal ontogeny between audition (+) and (-), unexpectedly, developmental regulation of gene expression dynamics is strictly conserved with age-locked trend in vocal motor circuit in both intact and deafened birds, indicating sensory-input independent robustness of developmental gene expression dynamics in the motor circuit for sensorimotor learning. This discrepancy between outward vocal phenotype and inward gene expression dynamics provides new insight into neural regulation at closing of the critical period for vocal learning by two different forms: auditory inputs-dependent ‘active’ crystallization and gene expression dynamics-mediated ‘passive’ crystallization.
2014-03-21 | GSE56075 | GEO
Project description:The sound of tape-recorded birdsong triggers a set of behavioral and physiological responses in zebra finches, including transcriptional activation of the zenk gene in the auditory forebrain. Song repetition leads to the stimulus-specific habituation of these responses. To gain insight into the mechanisms that couple auditory experience to gene regulation, we monitored the phosphorylation of the zebra finch extracellular signal-regulated kinase (ERK) protein by immunoblotting. Initial presentations of novel song (but not tones or noise) resulted in a rapid increase in ERK phosphorylation, followed by a return to basal levels within 5 min. This response was localized to the auditory forebrain where the zenk gene is activated. Sustained repetition of one song caused a selective habituation of the ERK response: a different song triggered another cycle of ERK phosphorylation without altering the habituated response to the first. To test directly for a role of ERK in experience-dependent zenk gene regulation, we infused an inhibitor of mitogen-activated and extracellular-regulated protein kinase kinase (MEK-1; the enzyme responsible for ERK activation) unilaterally into one auditory lobule just before song stimulation. The song-induced increase in zenk mRNA was blocked on the side of the injection, but not on the contralateral (uninfused) side. These results show that ERK phosphorylation is necessary for the initiation of the zenk gene response to novel song and identify ERK as a plausible site of signal integration underlying the selective habituation of genomic responses to a repeated song.
| S-EPMC6729643 | biostudies-literature
Project description:The arcopallium, a key avian forebrain region, receives inputs from numerous brain areas and is a major source of descending sensory and motor projections. While there is evidence of arcopallial subdivisions, the internal organization or the arcopallium is not well understood. The arcopallium is also considered the avian homologue of mammalian deep cortical layers and/or amygdalar subdivisions, but one-to-one correspondences are controversial. Here we present a molecular characterization of the arcopallium in the zebra finch, a passerine songbird species and a major model organism for vocal learning studies. Based on in situ hybridization for arcopallial-expressed transcripts (AQP1, C1QL3, CBLN2, CNTN4, CYP19A1, ESR1/2, FEZF2, MGP, NECAB2, PCP4, PVALB, SCN3B, SCUBE1, ZBTB20, and others) in comparison with cytoarchitectonic features, we have defined 20 distinct regions that can be grouped into six major domains (anterior, posterior, dorsal, ventral, medial, and intermediate arcopallium, respectively; AA, AP, AD, AV, AM, and AI). The data also help to establish the arcopallium as primarily pallial, support a unique topography of the arcopallium in passerines, highlight similarities between the vocal robust nucleus of the arcopallium (RA) and AI, and provide insights into the similarities and differences of cortical and amygdalar regions between birds and mammals. We also propose the use of AMV (instead of nucleus taenia/TnA), AMD, AD, and AI as initial steps toward a universal arcopallial nomenclature. Besides clarifying the internal organization of the arcopallium, the data provide a coherent basis for further functional and comparative studies of this complex avian brain region.
| S-EPMC6879308 | biostudies-literature
Project description:Recent evidence suggests that some sex differences in brain and behavior might result from direct genetic effects, and not solely the result of the organizational effects of steroid hormones. The present study examined the potential role for sex-biased gene expression during development of sexually dimorphic singing behavior and associated song nuclei in juvenile zebra finches.A microarray screen revealed more than 2400 putative genes (with a false discovery rate less than 0.05) exhibiting sex differences in the telencephalon of developing zebra finches. Increased expression in males was confirmed in 12 of 20 by qPCR using cDNA from the whole telencephalon; all of these appeared to be located on the Z sex chromosome. Six of the genes also showed increased expression in one or more of the song control nuclei of males at post-hatching day 25. Although the function of half of the genes is presently unknown, we have identified three as: 17-beta-hydroxysteroid dehydrogenase type IV, methylcrotonyl-CoA carboxylase, and sorting nexin 2.The data suggest potential influences of these genes in song learning and/or masculinization of song system morphology, both of which are occurring at this developmental stage.
| S-EPMC2664819 | biostudies-literature