Adult‐like neural representation of species‐specific songs in the auditory forebrain of zebra finch nestlings

The selectivity of neurons in the zebra finch auditory forebrain for natural sounds was investigated systematically. The principal auditory forebrain area in songbirds consists of the tonotopically organized field L complex, which, by its location in the auditory processing stream, can be compared with the auditory cortex of mammals. We also recorded from a secondary auditory area, cHV. Field L and cHV are auditory processing stages that are presynaptic to the specialized song system nuclei where auditory neurons show an extremely selective response for the bird's own song, but weak response to almost any other sounds, including conspecific songs. In our study, we found that neurons in field L and cHV had stronger responses to conspecific song than to synthetic sounds that were designed to match the lower order acoustical properties of song, such as their overall power spectra and AM spectra. Such preferential responses to natural sounds cannot be explained by linear frequency tuning or simple nonlinear intensity tuning and requires linear or nonlinear spectro-temporal neuronal transfer functions tuned to the acoustical properties of song. The selectivity for conspecific songs in field L and cHV might reflect an intermediate auditory processing stage for vocalizations that then contributes to the generation of the very specific selectivity for the bird's own song seen in the postsynaptic song system.

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Song Processing in the Zebra Finch Auditory Forebrain Reflects Asymmetric Sensitivity to Temporal and Spectral Structure

Frontiers in Neuroscience ◽

10.3389/fnins.2017.00549 ◽

2017 ◽

Vol 11 ◽

Cited By ~ 10

Author(s):

Lisbeth Van Ruijssevelt ◽

Stuart D. Washington ◽

Julie Hamaide ◽

Marleen Verhoye ◽

Georgios A. Keliris ◽

...

Keyword(s):

Zebra Finch ◽

Spectral Structure ◽

Auditory Forebrain

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Local inhibition modulates learning-dependent song encoding in the songbird auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00262.2012 ◽

2013 ◽

Vol 109 (3) ◽

pp. 721-733 ◽

Cited By ~ 13

Author(s):

Jason V. Thompson ◽

James M. Jeanne ◽

Timothy Q. Gentner

Keyword(s):

Neural Representation ◽

Response Patterns ◽

Acoustic Features ◽

European Starlings ◽

Local Inhibition ◽

Auditory Forebrain ◽

Inhibitory Modulation ◽

Auditory Cortices ◽

Caudomedial Nidopallium

Changes in inhibition during development are well documented, but the role of inhibition in adult learning-related plasticity is not understood. In songbirds, vocal recognition learning alters the neural representation of songs across the auditory forebrain, including the caudomedial nidopallium (NCM), a region analogous to mammalian secondary auditory cortices. Here, we block local inhibition with the iontophoretic application of gabazine, while simultaneously measuring song-evoked spiking activity in NCM of European starlings trained to recognize sets of conspecific songs. We find that local inhibition differentially suppresses the responses to learned and unfamiliar songs and enhances spike-rate differences between learned categories of songs. These learning-dependent response patterns emerge, in part, through inhibitory modulation of selectivity for song components and the masking of responses to specific acoustic features without altering spectrotemporal tuning. The results describe a novel form of inhibitory modulation of the encoding of learned categories and demonstrate that inhibition plays a central role in shaping the responses of neurons to learned, natural signals.

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Species-Specific Auditory Forebrain Responses to Non-Learned Vocalizations in Juvenile Blackbirds

Brain Behavior and Evolution ◽

10.1159/000489115 ◽

2018 ◽

Vol 91 (4) ◽

pp. 193-200 ◽

Cited By ~ 4

Author(s):

Kathleen S. Lynch ◽

Matthew I.M. Louder ◽

Mark E. Hauber

Keyword(s):

Parental Species ◽

Species Recognition ◽

Molothrus Ater ◽

Early Gene ◽

Acoustic Similarity ◽

Neural Responses ◽

Closely Related Species ◽

Auditory Forebrain ◽

Caudomedial Nidopallium ◽

Species Specific

Species recognition mediates the association of individuals with conspecifics. Learned cues often facilitate species recognition via early social experience with parents and siblings. Yet, in some songbirds, the production of species-typical vocalizations develops in the absence of early social experiences. Here, we investigate the auditory-evoked neural responses of juvenile red-winged blackbirds (Agelaius phoeniceus), a nonparasitic (parental) species within the Icterid family and contrast these results with a closely related Icterid parasitic species that lacks parental care, the brown-headed cowbird (Molothrus ater). We demonstrate that immediate early gene (IEG) activity in the caudomedial mesopallium (CMM) is selectively evoked in response to conspecific non-learned vocalizations in comparison to 2 types of heterospecific non-learned vocalizations, independent of the acoustic similarity patterns between the playback stimuli. This pattern, however, was not detected in the caudomedial nidopallium (NCM). Because the red-winged blackbird is a parental species, the conspecific non-learned vocalization is presumably a familiar sound to the juvenile red-winged blackbird, whereas the heterospecific non-learned vocalizations are novel. We contrast results reported here with our recent demonstration of selective IEG induction in response to non-learned conspecific vocalizations in juvenile parasitic brown-headed cowbirds, in which conspecific non-learned vocalizations are presumably novel. In this case, selective IEG induction from conspecific non-learned vocalization occurred within NCM but not within CMM. By comparing closely related species with stark differences in the early exposure to conspecifics, we demonstrate that CMM and NCM respond to familiar vs. novel non-learned vocalizations in a manner that parallel previously reported regional responses to learned vocalizations such as conspecific songs.

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Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

10.1101/657825 ◽

2019 ◽

Cited By ~ 2

Author(s):

Elliot A. Layden ◽

Kathryn E. Schertz ◽

Marc G. Berman ◽

Sarah E. London

Keyword(s):

Functional Connectivity ◽

Zebra Finch ◽

Resting State Fmri ◽

Zebra Finches ◽

Auditory Forebrain ◽

Sensory Learning ◽

Functional Connectivity Strength ◽

Caudomedial Nidopallium ◽

Single Cluster ◽

Connectivity Strength

AbstractMuch as humans acquire speech in early childhood, the zebra finch (Taeniopygia guttata) songbird learns to sing from an adult “tutor” during the first three months of life. Within a well-defined critical period (CP), juvenile zebra finches memorize a tutor song that will guide subsequent motor patterning. This sensory learning process is mediated by tutor experience-dependent neuroplasticity within the auditory forebrain. Here, we used longitudinal resting-state fMRI analyses to investigate whether tutor experience also modifies patterns of functional connectivity (FC) within the juvenile zebra finch brain. Eighteen male zebra finches (only males sing) were scanned before, during, and at the end of the CP, as well as at the young adult stage. Prior to the onset of the CP, birds were separated into rearing conditions: Normal (aviary-housed; N=5), Tutored (one adult male tutor and one adult female; N=7), and Isolate (two adult females, isolated from male song; N=6). Brain-wide voxel-wise analyses identified a single cluster overlapping the left caudomedial nidopallium (NCM) of the auditory forebrain that showed developmentally decreasing FC strength in Isolates but stable or increasing FC in Normal and Tutored birds. Additionally, FC between left NCM and left dorsal cerebellum showed a parallel developmental difference. Developmental changes in left NCM FC strength statistically mediated condition-related differences in song stereotypy. These results extend previous reports of tutor experience-dependent plasticity in NCM at epigenetic, genomic, molecular, and cellular levels to the whole-brain functional network level by demonstrating that tutor experience also influences the development of NCM FC. Moreover, these results link NCM FC to the emergence of song stereotypy.

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Song Tutor Choice in Zebra Finches and Bengalese Finches: the Relative Importance of Visual and Vocal Cues

Behaviour ◽

10.1163/156853988x00557 ◽

1988 ◽

Vol 104 (3-4) ◽

pp. 281-299 ◽

Cited By ~ 18

Author(s):

N.S. Clay-Ton

Keyword(s):

Zebra Finch ◽

Taeniopygia Guttata ◽

Song Learning ◽

The Other ◽

Zebra Finches ◽

Relative Importance ◽

Bengalese Finch ◽

Vocal Cues ◽

Species Specific ◽

Zebra Finch Song

AbstractThis paper examined the relative importance of visual and vocal cues for song tutor choice. In the first study zebra finches, Taeniopygia guttata, and Bengalese finches, Lonchura striata, were housed with two song tutors at independence, a zebra finch singing Bengalese finch song and a Bengalese finch singing zebra finch song. All the males tended to learn from the conspecific song tutor, irrespective of whether they had been raised by a pair of conspecifics, the female alone or cross-fostered to a pair of the other species. In the second study zebra finches were housed at independence with two conspecific song tutors, one with a normal song and one which sang Bengalese finch song elements. There was no tendency to learn zebra finch elements which suggests that species-specific elements are not important for song tutor choice in zebra finches. Other vocal differences between the tutors such as length of the song phrase and species-specific call notes might bias learning in favour of the conspecific. Visual differences between the two species, both in appearance and behaviour, seem to be important. Parental cues before independence appear to be relatively uninfluential. However, siblings may be important, both the species and number per clutch: this is a factor which has been overlooked in previous studies of song learning.

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