Our laboratory is broadly interested in understanding the neural mechanisms that control behavior – from the nature of the sensory and social cues that trigger the behavioral response to the neural commands that drive these specific behaviors. To address these questions, we study a highly conserved neural circuit in the songbird that is necessary for the production and learning of social communication signals. Our work is integrative in nature and therefore employs a range of different experimental approaches. These include behavioral analysis of social behavior in a natural context using advanced computer vision techniques, electrophysiological recording in awake behaving animals and anatomical characterization of the neural circuitry that underlie these behaviors.
As with all circuits that control behavior, the neural circuit we study can be divided into several different functional modules and our laboratory has performed studies at all levels of the circuit. These have included studies in (1) auditory forebrain areas that process vocal communication signals, (2) brainstem circuits that drive sexual posture and vocal-respiratory patterns and (3) the circuit module, known as the “song system”, that links the auditory forebrain to the brainstem and which is critical for conferring features to the behavior that include behavioral selectivity, context-specificity and learning. Figure 1 illustrates the modular organization of the neural circuit that controls song in male songbirds and highlights known and unknown connections within this circuit in the non-singing female brain.
In male songbirds, the discrete nature of the “song system” has provided a unique opportunity to link neural circuit dynamics to behavior because the highly stereotyped nature of the song, especially in the zebra finch, has allowed the ability to directly link neuronal events to individual behavioral gestures. Much of the work in the lab has taken advantage of this feature. Interestingly, female songbirds have the same identical neural circuit (although less pronounced in size) as the male, even in species such as the zebra finch or cowbird, where females do not sing! This raises the question, what role does this neural circuitry play in females?
Our recent findings suggest that the female “song system” controls song preference during courtship behavior. These findings have led the laboratory to pursue the hypothesis that the “song system” is a multifunctional circuit that controls courtship behavior more generally. Under this umbrella, male courtship behavior would include song and in females it would include the copulation solicitation display (CSD).
We have always focused exclusively on song and its neural control in the male and we have made significant contributions in this area. While still pursuing work on male song control, the lab has recently changed its research focus to investigate the role of the “song system” in controlling female sexual behavior. Using principles and techniques gathered from work in male songbirds, our current work aims to study female songbirds in an attempt to understand the neural control of courtship behavior.
Our current work can be divided into four major areas of investigation. Three of these areas focus on female courtship behavior. A fourth area continues our work on song control in males.
Toward a neural basis of courtship behavior and mate choice: Using female cowbirds (Molothrus ater), which do not sing but display a pronounced CSD when presented with male song, we are pursuing a multi-faceted approach to characterize the neural circuitry responsible for generating CSD behavior and its selectivity. This work involves (i) computer-vision aided behavioral quantification coupled with EMG recordings to generate a biomechanical model of the behavior, (ii) neural-recording in behaving birds from areas of the “song system” to establish motor correlates of CSD and (iii) neural recording in the auditory forebrain of behaving birds to seek a link between auditory selectivity and behavioral preference. [link]
- Computational ethology of female choice in a natural social context: Many species of songbirds are highly social and exhibit complex courtship behavior. Females typically must invest more in reproduction than males and therefore have strongincentives for selectivity in their mating choices. In a large collaborative effort involving several other biology and engineering labs, we are developing an observational arena in the form of a large outdoor aviary with an array of cameras and microphones to observe moment-to-moment behavioral interactions (vocal and gestural) within bird social groups. Computational and advanced network analyses will be used to quantify social interactions between individuals to develop predictive models of mate choice. Focusing primarily on female preference, we will use our computational description of social behavior to address how perturbations to targeted areas of a discrete neural circuit in the female disrupts female preference and social group dynamics. [link]
- Modulation of auditory and motor processing by social context: Social context can profoundly affect song characteristics in male songbirds. It also likely dramatically alters auditory processing in higher-order auditory/vocal control centers. We have performed a number of studies investigating the role and neural target of the neuromodulator norepinephrine in modulating auditory processing and song production. With the development of our behavioral arena for quantifying social behavior, we aim to record neural activity from birds interacting in a natural social context and quantify how neural characteristics, such as auditory responses to male song, can be shaped by the social context in which they are heard. [link]
- Neural control of song production and the role of vocal-respiratory feedback: Sensory activation of pressure and chemical receptors in the lungs and airsacs become activated during singing. We are testing the hypothesis that these viscerosensory (i.e. relayed through the vagus nerve) feedback signals get relayed back to forebrain centers that control song and are used by specialized basal ganglia circuits to maintain stable song output. The role of viscerosensory feedback in vocal motor control and its processing by basal ganglia circuits is poorly understood and remains largely underestimated despite possible links to a number of neurological disorders that include spasmodic dysphonia. [link]