Neural representation of spectral and temporal features of song in the auditory forebrain of zebra finches as revealed by functional MRI

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird’s own immature song) and the goal motor pattern (each bird’s adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird’s own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.

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Neural representation of abstract task structure during generalization

10.1101/2020.07.21.213009 ◽

2020 ◽

Author(s):

Avinash R. Vaidya ◽

Henry M. Jones ◽

Johanny Castillo ◽

David Badre

Keyword(s):

Prior Knowledge ◽

Functional Mri ◽

Neural Representation ◽

Human Cognition ◽

Neural Systems ◽

Task Structure ◽

Task Knowledge ◽

Additional Training ◽

Task Representations

AbstractAbstract task representations enable generalization, including inferring new behaviors based on prior knowledge without additional training. However, evidence for a neural representation that meets this benchmark is surprisingly limited. Here, using functional MRI (fMRI), we observed that abstract task structure was represented within frontoparietal networks during generalization. These results reveal the neural systems supporting a vital feature of human cognition: the abstraction of task knowledge to infer novel behaviors.

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Effect of Vocal Nerve Section on Song and ZENK Protein Expression in Area X in Adult Male Zebra Finches

Neural Plasticity ◽

10.1155/2012/902510 ◽

2012 ◽

Vol 2012 ◽

pp. 1-7 ◽

Cited By ~ 1

Author(s):

Congshu Liao ◽

Dongfeng Li

Keyword(s):

Protein Expression ◽

Adult Male ◽

Control Group ◽

Zebra Finches ◽

Nerve Section ◽

Singing Behavior ◽

Temporal Features ◽

The Right ◽

Area X ◽

The Relationship

ZENK expression in vocal nuclei is associated with singing behavior. Area X is an important nucleus for learning and stabilizing birdsong. ZENK expression is higher in Area X compared to that in other vocal nuclei when birds are singing. To reveal the relationship between the ZENK expression in Area X and song crystallization, immunohistochemistry was used to detect ZENK protein expression in Area X after the unilateral vocal nerve (tracheosyringeal nerve) section in adult male zebra finches. Sham operations had no effect on song. In contrast, section of unilateral vocal nerve could induce song decrystallization at the 7th day after the surgery. The spectral and the temporal features of birdsong were distorted more significantly in the right-side vocal nerve section than in the left-side vocal nerve section. In addition, after surgery, ZENK expression was higher in the right-side of Area X than in the left-side. These results indicate that the vocal nerve innervations probably are right-side dominant. ZENK expression in both sides of Area X decreased, as compared to control group after surgery, which suggests that the ZENK expression in Area X is related to birdsong crystallization, and that there is cooperation between the Area X in AFP and syrinx nerve.

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Neural representation of animacy in the early visual areas: A functional MRI study

Brain Research Bulletin ◽

10.1016/j.brainresbull.2009.03.007 ◽

2009 ◽

Vol 79 (5) ◽

pp. 271-280 ◽

Cited By ~ 8

Author(s):

Y. Morito ◽

H.C. Tanabe ◽

T. Kochiyama ◽

N. Sadato

Keyword(s):

Functional Mri ◽

Neural Representation ◽

Visual Areas ◽

Mri Study

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Auditory Forebrain Neurons Track Temporal Features of Time-Warped Natural Stimuli

Journal of the Association for Research in Otolaryngology ◽

10.1007/s10162-013-0418-8 ◽

2013 ◽

Vol 15 (1) ◽

pp. 131-138

Author(s):

Ross K. Maddox ◽

Kamal Sen ◽

Cyrus P. Billimoria

Keyword(s):

Natural Stimuli ◽

Auditory Forebrain ◽

Temporal Features ◽

Forebrain Neurons

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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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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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Level-Dependent Latency Shifts Quantified Through Binaural Processing

Journal of Neurophysiology ◽

10.1152/jn.00392.2010 ◽

2010 ◽

Vol 104 (4) ◽

pp. 2224-2235

Author(s):

Ida Siveke ◽

Christian Leibold ◽

Katharina Kaiser ◽

Benedikt Grothe ◽

Lutz Wiegrebe

Keyword(s):

Temporal Structure ◽

Temporal Integration ◽

Sound Level ◽

Neural Representation ◽

Interaural Time Differences ◽

Firing Threshold ◽

Temporal Precision ◽

Binaural Processing ◽

Electrophysiological Recordings ◽

Temporal Features

The mammalian binaural system compares the timing of monaural inputs with microsecond precision. This temporal precision is required for localizing sounds in azimuth. However, temporal features of the monaural inputs, in particular their latencies, highly depend on the overall sound level. In a combined psychophysical, electrophysiological, and modeling approach, we investigate how level-dependent latency shifts of the monaural responses are reflected in the perception and neural representation of interaural time differences. We exploit the sensitivity of the binaural system to the timing of high-frequency stimuli with binaurally incongruent envelopes. Using these novel stimuli, both the perceptually adjusted interaural time differences and the time differences extracted from electrophysiological recordings systematically depend on overall sound pressure level. The perceptual and electrophysiological time differences of the envelopes can be explained in an existing model of temporal integration only if a level-dependent firing threshold is added. Such an adjustment of firing threshold provides a temporally accurate neural code of the temporal structure of a stimulus and its binaural disparities independent of overall sound level.

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