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Roeser, A. C.

Publications and source records attributed to Roeser, A. C..

3 recordsLinked to original sources

The songbird lateral habenula projects to dopaminergic midbrain and is important for normal vocal development

Mistakes in performance feel disappointing, suggesting that brain pathways for aversive feedback may play a role in motor learning. Here we tested if the lateral habenula (LHb), an evolutionarily conserved part of the limbic system known in mammals to relay aversive feedback from ventral pallidum (VP) to ventral tegmental area (VTA) dopamine neurons, is involved in birdsong learning and production. By combining viral tract tracing and functional circuit mapping, we discovered that songbird LHb links VP and an auditory cortical area to singing-related DA neurons that signal song errors. As in mammals, VP stimulation activated LHb activity and LHb stimulation suppressed DA firing. To test this pathways role in learning we lesioned the LHb in juvenile zebra finches and recorded their songs in adulthood. Birds with the LHb lesioned as juveniles produced highly unusual vocalizations as adults, including prolonged high-pitch notes and species-atypical trills. These findings identify a songbird VP-LHb-VTA pathway with similar functional connectivity as mammals, expand the known territories of vocal learning circuits, and demonstrate that limbic circuits associated with disappointing outcomes are important for motor performance learning.

neuroscience↗

Movement signaling in ventral pallidum and dopaminergic midbrain is gated by behavioral state in singing birds

Movement-related neuronal discharge in ventral tegmental area (VTA) and ventral pallidum (VP) is inconsistently observed across studies. One possibility is that some neurons are movement-related and others are not. Another possibility is that the precise behavioral conditions matter - that a single neuron can be movement related under certain behavioral states but not others. We recorded single VTA and VP neurons in birds transitioning between singing and non-singing states, while monitoring body movement with microdrive-mounted accelerometers. Many VP and VTA neurons exhibited body movement-locked activity exclusively when the bird was not singing. During singing, VP and VTA neurons could switch off their tuning to body movement and become instead precisely time-locked to specific song syllables. These changes in neuronal tuning occurred rapidly at state boundaries. Our findings show that movement-related activity in limbic circuits can be gated by behavioral context. Significance statementNeural signals in the limbic system have long been known to represent body movements as well as reward. Here we show that single neurons dramatically change their tuning to movements when a bird starts to sing.

neuroscience↗

A circuit motif in the songbird basal ganglia for computing predicted performance quality

Ventral tegmental area (VTA) dopamine neurons signal prediction error, the difference between actual and predicted outcome, but it remains unclear how error is computed. Here we identify in songbirds a ventral basal ganglia (vBG) region that is required for song learning and that sends prediction error signals to VTA. During singing, vBG neurons heterogeneously encoded song timing, auditory error, predicted error, and the difference between the two (prediction error). Viral tracing revealed inputs to vBG from auditory and vocal motor thalamus, auditory and vocal motor cortex, and VTA. Our findings reveal a classic actor-critic circuit motif in which a ventral critic learns the prediction component of a prediction error signal that is relayed by VTA to a dorsal actor (the vocal motor BG nucleus Area X). A circuit motif for computing reward prediction error can compute predicted performance quality during motor sequence learning.

neuroscience↗