Songbirds
We use songbirds to investigate neural mechanisms of motor learning, performance evaluation, courtship and parenting
The spiking of a single dopamine neuron during singing (Gadagkar et al, Science 2016).
Songbirds and humans have similar brain circuits
Basal ganglia in birds and mammals
The basal ganglia thalamocortical circuit shown at left is an evolutionarily conserved brain pathway required for trial and error learning in humans and song learning in birds. This pathway is associated with movement disorders such as Parkinson’s, Huntington’s and dystonia, and psychiatric illnesses such as schizophrenia and addiction. In past work we discovered that the behavior-locked activity patterns of BG cell types is similar in singing birds and behaving primates.
The 'trial' part of learning: baby birds babble - and get better with practice
Trial and error song learning
Adult zebra finches sing a stereotyped song with a fixed sequence of syllables, e.g. 'a-b-c.' Juvenile finches hear their tutor song, and begin a month-long process to try to imitate it. Like babbling infants juveniles don't know how to move their vocal muscles to make the right sounds, so they 'babble.' Birds practice - singing thousands of songs per day - and gradually learn to imitate their tutors.
The 'error' part of learning: Birds get a spritz of dopamine when a they hit the right note
We discovered that when a singing bird unexpectedly hears itself sing the right note, its dopamine neurons are activated in the same way as when a thirsty monkey unexpectedly receives juice. And following song mistakes, its DA neurons are suppressed as when a primate experiences disappointing reward omission.
We discovered brain signals suggesting that songbirds know exactly when they are coming into a tricky part of their song
We discovered an actor-critic circuit motif, similar to one used in common deep reinforcement learning networks, inside the songbird basal ganglia. This motif computes dopaminergic performance error signal by comparing the actual (heard) to the predicted quality of individual song syllables.
Males turn off their dopaminergic self-evaluation signals when they perform for females
We discovered that dopamine signals are gated by social context. When a male courts a female, its DA neurons no longer respond to his errors. They are instead activated by her vocal calls.
It was long assumed that a main function of dopamine in the songbird was to facilitate the reduction in variability that occurs when a lone male bird transitions to female-directed song performance. We recorded from dopamine neurons during female-directed singing and made three surprising discoveries. First, tonic discharge of DA neurons did not change with the appearance of the female, countering decades of untested assumptions about activation of dopamine neurons by mating contexts. Second, DA performance error signals that were present when males sang alone mostly disappeared when males sang to females, demonstrating that DA error signals can be dynamically gated. Third, this gating suggested that during courtship the male attended less to evaluating his own song and more to the behavior of the female. Consistent with this idea, we found that DA neurons were activated by female vocalizations, providing the first demonstration that DA can by activated by the vocalization of a conspecific. In ongoing work, we are testing how DA signal gating is implemented in upstream circuits.