The songs of mature zebra finches are notoriously repetitious, or 'crystallized'. Despite this stability, new work reveals that chronic pharmacologically driven bursting of cortical inputs to the basal ganglia can drive cumulative and lasting changes to multiple vocal features, including phenomena reminiscent of human stuttering.

Behavioral variability is thought to be critical for trial and error learning, but where such motor exploration is generated in the central nervous system is unclear. The zebra finch songbird species offers a highly appropriate model in which to address this question. The male song is amenable to detailed measurements of variability, while the brain contains an identified cortico-basal ganglia loop that underlies this behavior. We used pharmacogenetic interventions to separately interrogate cortical and basal ganglia nodes of zebra finch song control circuitry. We show that bidirectional manipulations of each node produce near mirror image changes in vocal control: Cortical activity promotes song variability, whereas basal ganglia activity promotes song stability. Furthermore, female conspecifics can detect these pharmacogenetically elicited changes in song quality. Our results indicate that cortex and striatopallidum can jointly and reciprocally affect behaviorally relevant levels of vocal variability, and point to endogenous mechanisms for its control.

Background

Assessing the active space of the various types of information encoded by songbirds' vocalizations is important to address questions related to species ecology (e.g. spacing of individuals), as well as social behavior (e.g. territorial and/or mating strategies). Up to now, most of the previous studies have investigated the degradation of species-specific related information (species identity), and there is a gap of knowledge of how finer-grained information (e.g. individual identity) can transmit through the environment. Here we studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation.

Methodology

We performed sound transmission experiments of zebra finches' distance calls at various propagation distances. The propagated calls were analyzed using discriminant function analyses on a set of analytical parameters describing separately the spectral and temporal envelopes, as well as on a complete spectrographic representation of the signals.

Results/conclusion

We found that individual signature is remarkably resistant to propagation as caller identity can be recovered even at distances greater than a hundred meters. Male calls show stronger discriminability at long distances than female calls, and this difference can be explained by the more pronounced frequency modulation found in their calls. In both sexes, individual information is carried redundantly using multiple acoustical features. Interestingly, features providing the highest discrimination at short distances are not the same ones that provide the highest discrimination at long distances.

Behavioral variability is thought to be critical for trial and error learning, but where such motor exploration is generated in the central nervous system is unclear. The zebra finch songbird species offers a highly appropriate model in which to address this question. The male song is amenable to detailed measurements of variability, while the brain contains an identified cortico-basal ganglia loop that underlies this behavior. We used pharmacogenetic interventions to separately interrogate cortical and basal ganglia nodes of zebra finch song control circuitry. We show that bidirectional manipulations of each node produce near mirror image changes in vocal control: Cortical activity promotes song variability, whereas basal ganglia activity promotes song stability. Furthermore, female conspecifics can detect these pharmacogenetically elicited changes in song quality. Our results indicate that cortex and striatopallidum can jointly and reciprocally affect behaviorally relevant levels of vocal variability, and point to endogenous mechanisms for its control.