Dataset Information

Emergence of learned categorical representations within an auditory forebrain circuit.

ABSTRACT: Many learned behaviors are thought to require the activity of high-level neurons that represent categories of complex signals, such as familiar faces or native speech sounds. How these complex, experience-dependent neural responses emerge within the brain's circuitry is not well understood. The caudomedial mesopallium (CMM), a secondary auditory region in the songbird brain, contains neurons that respond to specific combinations of song components and respond preferentially to the songs that birds have learned to recognize. Here, we examine the transformation of these learned responses across a broader forebrain circuit that includes the caudolateral mesopallium (CLM), an auditory region that provides input to CMM. We recorded extracellular single-unit activity in CLM and CMM in European starlings trained to recognize sets of conspecific songs and compared multiple encoding properties of neurons between these regions. We find that the responses of CMM neurons are more selective between song components, convey more information about song components, and are more variable over repeated components than the responses of CLM neurons. While learning enhances neural encoding of song components in both regions, CMM neurons encode more information about the learned categories associated with songs than do CLM neurons. Collectively, these data suggest that CLM and CMM are part of a functional sensory hierarchy that is modified by learning to yield representations of natural vocal signals that are increasingly informative with respect to behavior.

SUBMITTER: Jeanne JM

PROVIDER: S-EPMC3060658 | biostudies-other | 2011 Feb

REPOSITORIES: biostudies-other

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Emergence of learned categorical representations within an auditory forebrain circuit.

Jeanne James M JM Thompson Jason V JV Sharpee Tatyana O TO Gentner Timothy Q TQ

The Journal of neuroscience : the official journal of the Society for Neuroscience 20110201 7

Many learned behaviors are thought to require the activity of high-level neurons that represent categories of complex signals, such as familiar faces or native speech sounds. How these complex, experience-dependent neural responses emerge within the brain's circuitry is not well understood. The caudomedial mesopallium (CMM), a secondary auditory region in the songbird brain, contains neurons that respond to specific combinations of song components and respond preferentially to the songs that bir ...[more]

PMID: 21325527

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Project description:The brain transforms continuous acoustic events into discrete category representations to downsample the speech signal for our perceptual-cognitive systems. Such phonetic categories are highly malleable, and their percepts can change depending on surrounding stimulus context. Previous work suggests these acoustic-phonetic mapping and perceptual warping of speech emerge in the brain no earlier than auditory cortex. Here, we examined whether these auditory-category phenomena inherent to speech perception occur even earlier in the human brain, at the level of auditory brainstem. We recorded speech-evoked frequency following responses (FFRs) during a task designed to induce more/less warping of listeners' perceptual categories depending on stimulus presentation order of a speech continuum (random, forward, backward directions). We used a novel clustered stimulus paradigm to rapidly record the high trial counts needed for FFRs concurrent with active behavioral tasks. We found serial stimulus order caused perceptual shifts (hysteresis) near listeners' category boundary confirming identical speech tokens are perceived differentially depending on stimulus context. Critically, we further show neural FFRs during active (but not passive) listening are enhanced for prototypical vs. category-ambiguous tokens and are biased in the direction of listeners' phonetic label even for acoustically-identical speech stimuli. These findings were not observed in the stimulus acoustics nor model FFR responses generated via a computational model of cochlear and auditory nerve transduction, confirming a central origin to the effects. Our data reveal FFRs carry category-level information and suggest top-down processing actively shapes the neural encoding and categorization of speech at subcortical levels. These findings suggest the acoustic-phonetic mapping and perceptual warping in speech perception occur surprisingly early along the auditory neuroaxis, which might aid understanding by reducing ambiguity inherent to the speech signal.

Project description:BackgroundThe maturation of the brain involves the coordinated expression of thousands of genes, proteins and regulatory elements over time. In sensory pathways, gene expression profiles are modified by age and sensory experience in a manner that differs between brain regions and cell types. In the auditory system of altricial animals, neuronal activity increases markedly after the opening of the ear canals, initiating events that culminate in the maturation of auditory circuitry in the brain. This window provides a unique opportunity to study how gene expression patterns are modified by the onset of sensory experience through maturity. As a tool for capturing these features, next-generation sequencing of total RNA (RNAseq) has tremendous utility, because the entire transcriptome can be screened to index expression of any gene. To date, whole transcriptome profiles have not been generated for any central auditory structure in any species at any age. In the present study, RNAseq was used to profile two regions of the mouse auditory forebrain (A1, primary auditory cortex; MG, medial geniculate) at key stages of postnatal development (P7, P14, P21, adult) before and after the onset of hearing (~P12). Hierarchical clustering, differential expression, and functional geneset enrichment analyses (GSEA) were used to profile the expression patterns of all genes. Selected genesets related to neurotransmission, developmental plasticity, critical periods and brain structure were highlighted. An accessible repository of the entire dataset was also constructed that permits extraction and screening of all data from the global through single-gene levels. To our knowledge, this is the first whole transcriptome sequencing study of the forebrain of any mammalian sensory system. Although the data are most relevant for the auditory system, they are generally applicable to forebrain structures in the visual and somatosensory systems, as well.ResultsThe main findings were: (1) Global gene expression patterns were tightly clustered by postnatal age and brain region; (2) comparing A1 and MG, the total numbers of differentially expressed genes were comparable from P7 to P21, then dropped to nearly half by adulthood; (3) comparing successive age groups, the greatest numbers of differentially expressed genes were found between P7 and P14 in both regions, followed by a steady decline in numbers with age; (4) maturational trajectories in expression levels varied at the single gene level (increasing, decreasing, static, other); (5) between regions, the profiles of single genes were often asymmetric; (6) GSEA revealed that genesets related to neural activity and plasticity were typically upregulated from P7 to adult, while those related to structure tended to be downregulated; (7) GSEA and pathways analysis of selected functional networks were not predictive of expression patterns in the auditory forebrain for all genes, reflecting regional specificity at the single gene level.ConclusionsGene expression in the auditory forebrain during postnatal development is in constant flux and becomes increasingly stable with age. Maturational changes are evident at the global through single gene levels. Transcriptome profiles in A1 and MG are distinct at all ages, and differ from other brain regions. The database generated by this study provides a rich foundation for the identification of novel developmental biomarkers, functional gene pathways, and targeted studies of postnatal maturation in the auditory forebrain.

Dataset Information

Emergence of learned categorical representations within an auditory forebrain circuit.

Publications

Emergence of learned categorical representations within an auditory forebrain circuit.

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