Social context differentially modulates activity of two interneuron populations in an avian basal ganglia nucleus

Abstract

Basal ganglia circuits are critical for the modulation of motor performance across behavioral states. In zebra finches, a cortical-basal ganglia circuit dedicated to singing is necessary for males to adjust their song performance and transition between spontaneous singing, when they are alone ("undirected" song), and a performance state, when they sing to a female ("female-directed" song). However, we know little about the role of different basal ganglia cell types in this behavioral transition or the degree to which behavioral context modulates the activity of different neuron classes. To investigate whether interneurons in the songbird basal ganglia encode information about behavioral state, I recorded from two interneuron types, fast-spiking interneurons (FSI) and external pallidal (GPe) neurons, in the songbird basal ganglia nucleus area X during both female-directed and undirected singing. Both cell types exhibited higher firing rates, more frequent bursting, and greater trial-by-trial variability in firing when male zebra finches produced undirected songs compared with when they produced female-directed songs. However, the magnitude and direction of changes to the firing rate, bursting, and variability of spiking between when birds sat silently and when they sang undirected and female-directed song varied between FSI and GPe neurons. These data indicate that social modulation of activity important for eliciting changes in behavioral state is present in multiple cell types within area X and suggests that social interactions may adjust circuit dynamics during singing at multiple points within the circuit.

Keywords: basal ganglia; electrophysiology; globus pallidus; songbird; striatum.

Fig. 1.

Song system. A: diagram of connections between the anterior forebrain pathway and motor pathway with reference to similar structures in mammals. HVC, proper name; RA, robust nucleus of the arcopallium; LMAN, lateral magnocellular nucleus of the anterior nidopallium; DLM, medial nucleus of the dorsolateral thalamus. B: connections among different striatal (shaded circles) and pallidal cell types (open circles) in the avian basal ganglia nucleus area X. Dashed lines indicate hypothesized connections, lines ending in arrows indicate excitatory connections, and lines ending in solid circles are inhibitory connections. FSI, fast-spiking interneuron; SN, medium spiny neuron; GPe, external globus pallidus neuron; GPi, internal globus pallidus neuron.

Fig. 2.

Social modulation of activity in 2 interneuron types. A and B: raw traces of singing-related activity during a bout of female-directed (A) and undirected singing (B) in an FSI neuron. Top panel of each is a spectrogram of the song. C: spectrogram of a single female-directed motif (FD; top) and undirected motif (UD; bottom). D: raster plots of activity during the motif for FD (top) and UD (middle) singing and during an equivalent duration of silence (SP; bottom). E: peristimulus time histogram (PSTH) of the motif-related activity shown in D. F–J: examples of the same singing-related and spontaneous activity in a GPe neuron.

Fig. 3.

Social context differentially affects the rate and regularity of firing in FSI and GPe neurons. A and B: interspike interval (ISI) plots for FSI and GPe neurons, respectively, during spontaneous (SP) activity and during female-directed (FD) and undirected singing (UD). C: in FSI neurons, firing rates are increased during UD singing. D: firing rates in GPe neurons are increased during UD singing and either unchanged or decreased during FD singing relative to SP activity. The coefficient of variation (CV) of the ISI was highest during UD singing in both FSI (E) and GPe (F) neurons. In GPe neurons (F), the CV of the ISI was also significantly higher during FD singing than during SP activity. G: the CV2 of spiking in FSI neurons was not significantly different (NS) between SP, FD, and UD birds. H: in contrast, the CV2 of GPe neurons increased during both FD and UD singing compared with the tonic and regular firing during SP activity. *P < 0.05.

Fig. 4.

Social context differentially modulates spike statistics in FSI and GPe neurons. A: examples of the autocorrelation functions for single FSI (top) and GPe neurons (bottom) during undirected singing (UD; dark blue line), female-directed singing (FD; light blue line), and spontaneous activity (SP; gray line) highlighting the differences between cell types and social context in the correlations. B: autocorrelation functions for all FSI (top) and GPe neurons (bottom) for UD (dark blue), FD (light blue), and SP (gray). Dark lines indicate the mean and shading represents the SD. C: differences in the peak of the autocorrelation functions distinguish between social contexts in each cell type and between cell type functions during FD singing. ^a,b,cP < 0.05, groups not indicated by the same letter are significantly different from each other. D: GPe and FSI neurons also differed in the width of the autocorrelation function during UD singing, measured as the latency to reach Poisson firing. *P < 0.05.

Fig. 5.

Social context and cell type affect trial-by-trial variability. The stereotypy of firing across trials, as measured by the trial-by-trial cross correlation (CC), was significantly higher during female-directed (FD) than undirected (UD) singing in both FSI (A) and GPe (B) neurons. C and D: the greater variability during UD song resulted from increased variability of isolated spikes as well as bursts. The peak trial-by-trial CC was not different between undirected spike trains, isolated spikes, or burst onsets in FSI (C) and GPe neurons (D). In addition, values for all three were higher than for randomly circularly shifted data (shading near 0 represents mean + SD for shifted data) and lower than the trial-by-trial CC for FD singing (long-dashed line). E: correlation coefficients between the average PSTH during female-directed and undirected singing for all FSI and GPe neurons. All correlation coefficients were significantly higher than the mean (dashed line) + 2SD (gray shaded area) for randomly circularly shifted data. However, FSI and GPe neurons were not different. * P < 0.05.