Neurons in a Forebrain Nucleus Required for Vocal Plasticity Rapidly Switch between Precise Firing and Variable Bursting Depending on Social Context

Abstract

Song is a learned vocal behavior influenced by social interactions. Prior work has suggested that the anterior forebrain pathway (AFP), a specialized pallial-basal ganglia circuit critical for vocal plasticity, mediates the influence of social signals on song. Here, we investigate the signals the AFP sends to song motor areas and their dependence on social context by characterizing singing-related activity of single neurons in the AFP output nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium). We show that interaction with females causes marked, real-time changes in firing properties of individual LMAN neurons. When males sing to females ("directed"), LMAN neurons exhibit reliable firing of single spikes precisely locked to song. In contrast, when males sing alone ("undirected"), the same LMAN neurons exhibit prominent burst firing and trial-by-trial variability. Burst structure and timing vary substantially across repeated undirected trials. Despite context-dependent differences in firing statistics, the average pattern of song-locked firing for an individual neuron is similar across behavioral contexts, suggesting a common underlying signal. Different LMAN neurons in the same bird, however, exhibit distinct firing patterns, suggesting that subsets of neurons jointly encode song features. Together, our findings demonstrate that behavioral interactions reversibly transform the signaling mode of LMAN neurons. Such changes may contribute to rapid switching of motor activity between variable and precise states. More generally, our results suggest that pallial-basal ganglia circuits contribute to motor learning and production through multiple mechanisms: patterned signals could guide changes in motor output while state-dependent variability could subserve motor exploration.

Task-related “cortical” bursting depends critically on basal ganglia input and is linked to vocal plasticity

“…Previous work has shown that acute inactivation of Area X in anesthetized adult zebra finches tonically disinhibits thalamic neurons, inducing higher spontaneous firing rates in LMAN (34), consistent with findings in mammals (8,35). According to firing-rate models of basal ganglia function, lesions of Area X should increase spontaneous firing rates in LMAN, which, in turn, could mask the normal singing-related rate increases observed in intact birds (36)(37)(38). Alternatively, lesions of Area X could change the firing statistics of LMAN neurons, as predicted by firing-pattern models, with or without affecting their overall firing rates.…”

“…In both intact and deaf birds, LMAN neurons increase their discharge before and during singing, consistent with premotor signaling (36)(37)(38). In the absence of Area X, we found that LMAN neurons continued to exhibit robust increases in firing rate before song initiation and during singing (Fig.…”

“…Previous studies have shown that LMAN neurons in intact birds typically fire brief, high-frequency bursts of action potentials when they sing alone (Fig. 3B, Left) (36,37). This result is characterized by a prominent peak at short intervals (∼2-3 ms) in the distribution of interspike intervals (ISI) (Fig.…”

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

“…A transition to neuronal burst firing has emerged as a unique mode of sensorimotor information transfer in the forebrain of songbirds and other vertebrates (20,(22)(23)(24)(25)(26). Burst firing has been associated with increased attention/wakefulness (23,27,28), synaptic efficacy (29,30), and discrimination among sensory stimuli (20,24,28) and is thought to depend on the activity of projections from the basal forebrain (e.g., cholinergic projections; ref.…”

“…To evaluate this elevation in burst firing, a custom software script for burst identification and analysis (CED) was used to process spike trains for bursts consisting of three or more action potentials separated by ≤10 ms (for similar burst parameters, see ref. 25). Burst parameters were quantified in response to each playback stimulus (30 iterations) for both estradiol and FAD experiments as described for spike rate data above.…”