Recurrent interactions between the input and output of a songbird cortico-basal ganglia pathway are implicated in vocal sequence variability.
Complex brain functions, such as the capacity to learn and modulate vocal sequences, depend on activity propagation in highly distributed neural networks. To explore the synaptic basis of activity propagation in such networks, we made dual in vivo intracellular recordings in anesthetized zebra finches from the input (nucleus HVC, used here as a proper name) and output [lateral magnocellular nucleus of the anterior nidopallium (LMAN)] neurons of a songbird cortico-basal ganglia (BG) pathway necessary to the learning and modulation of vocal motor sequences. These recordings reveal evidence of bidirectional interactions, rather than only feedforward propagation of activity from HVC to LMAN, as had been previously supposed. A combination of dual and triple recording configurations and pharmacological manipulations was used to map out circuitry by which activity propagates from LMAN to HVC. These experiments indicate that activity travels to HVC through at least two independent ipsilateral pathways, one of which involves fast signaling through a midbrain dopaminergic cell group, reminiscent of recurrent mesocortical loops described in mammals. We then used in vivo pharmacological manipulations to establish that augmented LMAN activity is sufficient to restore high levels of sequence variability in adult birds, suggesting that recurrent interactions through highly distributed forebrain-midbrain pathways can modulate learned vocal sequences.
Department of Neurobiology, Duke University, Durham, North Carolina 27710, USA.
Kosuke
K
Hamaguchi
Richard
R
Mooney
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000779:Anesthetics, Local / Q000494:pharmacology; D000818:Animals; D001640:Bicuculline / Q000031:analogs & derivatives / Q000494:pharmacology; D001703:Biophysics; D002452:Cell Count; D002540:Cerebral Cortex / Q000166:cytology / Q000187:drug effects / Q000502:physiology*; D004299:Dopamine beta-Hydroxylase / Q000378:metabolism; D059290:Dopaminergic Neurons / Q000502:physiology; D004558:Electric Stimulation; D007839:Functional Laterality; D018755:GABA Agonists / Q000494:pharmacology; D058787:GABA-A Receptor Antagonists / Q000494:pharmacology; D053400:High Vocal Center / Q000166:cytology / Q000293:injuries / Q000502:physiology*; D007051:Ibotenic Acid; D008012:Lidocaine / Q000494:pharmacology; D049408:Luminescent Agents / Q000378:metabolism; D008297:Male; D017551:Microdialysis; D009118:Muscimol / Q000494:pharmacology; D009434:Neural Pathways / Q000502:physiology*; D020308:Songbirds / Q000502:physiology*; D018709:Statistics, Nonparametric; D014446:Tyrosine 3-Monooxygenase / Q000378:metabolism; D014828:Vocalization, Animal / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000494:pharmacology
D000779:Anesthetics, Local; D018755:GABA Agonists; D058787:GABA-A Receptor Antagonists; D049408:Luminescent Agents; D007051:Ibotenic Acid; D009118:Muscimol; C017069:bicuculline methiodide; D005680:gamma-Aminobutyric Acid; D008012:Lidocaine; D014446:Tyrosine 3-Monooxygenase; D004299:Dopamine beta-Hydroxylase; D001640:Bicuculline