4. Neural control of song production and the role of vocal-respiratory feedback:

Previous accomplishments: Much of the field had assumed that song output was controlled by a hierarchically organized descending pathway. Based on some of our work (Schmidt, 2003), we proposed an alternate model that suggested an organization that was recurrent in nature (Schmidt et al., 2004, 2008). In this scheme, no single brain area is “at the top” of the circuit and motor commands are distributed throughout forebrain and brainstem (figure 4). Our model has gained significant traction in the field. Interestingly, this model was derived by a need to describe how songbirds, despite lacking connections (corpus callosum) between hemisphere, manage to coordinate and synchronize neural activity between hemispheres (Schmidt, 2003; Schmidt, 2008). This work also led us to investigate the role of the respiratory brainstem (n. Paraambigualis; PAm) as a neural substrate for bilateral coordination of motor commands during singing (Ashmore et al., 2005, 2008a, b) and led to the first detailed characterization of the avian respiratory brainstem (McLean et al., 2013). The unique perspective that the respiratory brainstem does more than just control breathing and that it might also be critical for sending bottom-up commands to the forebrain led to several invited reviews in the area of respiratory physiology (Schmidt et al., 2012; Schmidt and Goller, 2016; Schmidt and Wild, 2014).


Current studies: Our work identified the importance of bottom-up projections from the respiratory brainstem to forebrain song control areas, but the nature of these commands remains unclear. Because lesions of the thalamic relay nucleus Uvaeformis (Uva), which acts as a relay between respiratory brainstem and HVC, completely disrupts song production, most of the field has assumed that these commands are motor in nature. We have preliminary findings that imply that UVa carries sensory rather than motor information. Our hypothesis that bottom-up projections send sensory information to the forebrain is consistent with the anatomical placement of Uva within sensory thalamus and with the notion that the respiratory brainstem receives sensory inputs from sensors in the airsacs, lungs and possibly also the vocal musculature.  This bottom-up pathway could therefore play a critical role in providing sensory feedback from the vocal-respiratory apparatus to forebrain song control nuclei. Our current work supports this idea because activation of receptors in the airsacs can elicit robust, short latency (30 msec) neural responses in HVC (Burke et al., 2017). Our current work is focused on investigating the effects on behavior and HVC neural activity of targeted disruption of this sensory pathway using a number of different approaches which include, direct stimulation of air sacs, stimulation of the vagus nerve with polyimide thin film nanoclip stimulating electrodes (in collaboration with Tim Otchy, Boston University) [LINK] or stimulation of the respiratory brainstem.


Future directions: The role of basal ganglia circuits in vocal learning and maintenance in the songbird is well established and much evidence exists showing that it is involved in dopamine-dependent performance prediction error. Interestingly, all of the work has focused on error correction based on auditory feedback. Because basal ganglia circuits integrate many different types of sensory inputs, our future work will investigate the role of basal ganglia in processing sensory feedback signals from the vocal-respiratory apparatus and address how this circuit uses this information to modify song output during learning and maintenance.