Is neurogenesis in two songbird species related to their song sequence variability?

Neurogenesis takes part in the adult songbird brain and new neurons are integrated into the forebrain including defined areas involved in the control of song learning and production. It has been suggested that the new neurons in the song system might enable vocal variability. Here, we examined the basal levels of neurogenesis in two songbird species, zebra finch ( Taeniopygia guttata ) and Bengalese finch ( Lonchura striata var. domestica ), which do not learn new song elements as adults but differ in the level of song sequence variability. We found that Bengalese finches had less linear and stereotyped song sequence and a higher number of newborn cells in the neurogenic subventricular zone (SVZ) as well as the number of newly born neurons incorporated into the vocal nucleus HVC (used as a proper name) in comparison to zebra finches. Importantly, this vocal sequence variability in Bengalese finches correlated with the number of new neurons in the vocal nucleus HVC and more plastic song was associated with higher neuronal incorporation. In summary, our data support the hypothesis that newly generated neurons facilitate behavioural variability.

FoxP2 isoforms delineate spatiotemporal transcriptional networks for vocal learning in the zebra finch

Human speech is one of the few examples of vocal learning among mammals yet ~half of avian species exhibit this ability. Its neurogenetic basis is largely unknown beyond a shared requirement for FoxP2 in both humans and zebra finches. We manipulated FoxP2 isoforms in Area X, a song-specific region of the avian striatopallidum analogous to human anterior striatum, during a critical period for song development. We delineate, for the first time, unique contributions of each isoform to vocal learning. Weighted gene coexpression network analysis of RNA-seq data revealed gene modules correlated to singing, learning, or vocal variability. Coexpression related to singing was found in juvenile and adult Area X whereas coexpression correlated to learning was unique to juveniles. The confluence of learning and singing coexpression in juvenile Area X may underscore molecular processes that drive vocal learning in young zebra finches and, by analogy, humans.

Dopaminergic modulation of basal ganglia output through coupled excitation–inhibition

Learning and maintenance of skilled movements require exploration of motor space and selection of appropriate actions. Vocal learning and social context-dependent plasticity in songbirds depend on a basal ganglia circuit, which actively generates vocal variability. Dopamine in the basal ganglia reduces trial-to-trial neural variability when the bird engages in courtship song. Here, we present evidence for a unique, tonically active, excitatory interneuron in the songbird basal ganglia that makes strong synaptic connections onto output pallidal neurons, often linked in time with inhibitory events. Dopamine receptor activity modulates the coupling of these excitatory and inhibitory events in vitro, which results in a dynamic change in the synchrony of a modeled population of basal ganglia output neurons receiving excitatory and inhibitory inputs. The excitatory interneuron thus serves as one biophysical mechanism for the introduction or modulation of neural variability in this circuit.

A neural circuit mechanism for regulating vocal variability during song learning in zebra finches

Motor skill learning is characterized by improved performance and reduced motor variability. The neural mechanisms that couple skill level and variability, however, are not known. The zebra finch, a songbird, presents a unique opportunity to address this question because production of learned song and induction of vocal variability are instantiated in distinct circuits that converge on a motor cortex analogue controlling vocal output. To probe the interplay between learning and variability, we made intracellular recordings from neurons in this area, characterizing how their inputs from the functionally distinct pathways change throughout song development. We found that inputs that drive stereotyped song-patterns are strengthened and pruned, while inputs that induce variability remain unchanged. A simple network model showed that strengthening and pruning of action-specific connections reduces the sensitivity of motor control circuits to variable input and neural ‘noise’. This identifies a simple and general mechanism for learning-related regulation of motor variability.