1. Toward a neural basis of courtship behavior and mate choice:

Previous accomplishments: Unlike lordosis, which requires activation of somatosensory inputs typically achieved by rubbing the animal’s flanks, the CSD response in songbirds (figure 2) can be elicited by auditory stimulation alone. During CSD, the female arches her back to raise her torso, and spread the posterior feathers to expose her cloaca, a common orifice that serves as the only opening for the reproductive as well as the digestive and urinary tracts. Although CSD activation during normal courtship is likely modulated by visual cues as well, experimental presentation of male song is sufficient to elicit this distinctive behavior, even when the female is placed in a relatively small sound proof chamber. A striking feature of this behavior is that female cowbirds exhibit a great degree of selectivity in their behavior, consistently responding only to some songs and not others. In a collaborative study with David White (Wilfrid Laurier University, Ontario, CA) [LINK], we tested the hypothesis that part of the song system in the female cowbird is responsible for this selectivity. We showed that targeted lesions to nucleus HVC, a nucleus necessary for singing in males, causes a complete loss in response selectivity with the female going into posture to all songs that are presented to her (Maguire et al., 2013). These findings set the stage for the hypothesis that the song system is necessary in determining behavioral selectivity of the CSD response.


Current studies: With the goal of establishing the female cowbird as a model species for studying the role of the song system in the control and selectivity of the CSD response, we are using an integrative approach to quantify the circuitry, behavior and neural correlates. This work is currently funded by an NSF grant IOS 1557499: Neural Bases of Song Preference and Reproductive Behavior in a Female Songbird. Circuitry: In collaboration with Martin Wild (University of Auckland, NZ), we are defining the detailed pathways of the song system in the female cowbird. This includes auditory inputs into “song system” nuclei, connectivity within the “song system” and motor output including the specific motor neuron pools in the spinal cord. This fundamental circuitry work is essential for establishing the system as one that can be used to assess the involvement of the “song system” in courtship behavior. Our work so far has confirmed that certain song control nuclei are linked to the same basal ganglia circuits that are necessary for song learning and that the motor output of the circuit includes projections to the sacral motor neurons that innervate the cloaca, a muscle sphincter that is involved in copulation. Behavior: To provide the precise behavioral quantification necessary to link neural activity to precise segments of the copulatory behavior, we reasoned that manual segmentation of video would be insufficient.  Thus, in an extensive collaboration with the Daniilidis lab of the engineering department at Penn [LINK], we have developed and are employing cutting-edge computer vision approaches to segment CSD posture into precise time epochs that will allow for a precise quantification of the behavior. These analyses are coupled with physiological measurements such as muscle EMG as well as air pressure recording to provide a better biomechanical understanding of the behavior. In addition to facilitating alignment of neural activity to the behavior, these measurements will be used to quantify behavioral features such as latency, 3-D pose trajectory under different behavioral conditions. Neurophysiology: To properly characterize and link neural properties to behavioral, we considered that we require long-term recording technology.  Thus, we implemented carbon fiber recording technology in collaboration with the Gardner lab (Boston University) to allow long-term chronic neural recording in behaving cowbirds. This allows us to record for many weeks at a time from song control nuclei, a feature that is critical when testing for song preference because songs can only be presented every 1.5 hours to avoid behavioral habituation. Our current recordings are focused on the song motor nucleus RA, a possible homologue of primary motor cortex that projects directly to brainstem premotor neuron pools hypothesized to be associated with CSD. Our goal is to establish a neural correlate of CSD and compare/contrast neural dynamics in this structure to those observed in males during singing.


Future directions: Our initial studies have provided us with the ability to record long-term during behavioral sessions and detail the behavior in quantitative manner. Thus, we are now in a position to use this system to illuminate how the song system circuits modulates the behavior.  While most of our neural recordings are focused on RA, future studies will explore the neural correlates of song preference by recording in auditory forebrain as well as sensorimotor structures such as NIf and HVC. Because structures such as HVC in the female are thin and close to the dorsal surface, we will develop imaging methods (e.g. GCaMP) to record neural activity during CSD. An intriguing feature of the circuit is that the same specialized basal ganglia circuits necessary for song learning also are present in the female cowbird. Recording from these areas will allow us to evaluate the role of basal ganglia in action selection as it relates to song preference and compare/contrast its function with that observed in males during singing.