With the exception of relatively simple rhythmic motor patterns, models of motor control often place most of their emphasis on the telencephalon. This is certainly true for the production of learned vocal behaviors where the brainstem is viewed primarily as an output pathway for motor commands generated in the forebrain. With the recent exception of the motor control of eye movement, little is known about how brainstem nuclei involved in motor output might directly influence the generation of motor commands in the telencephalon. The experiments described in this proposal are aimed at elucidating the role of the respiratory brainstem in song pattern generation and more generally how the brainstem influences motor command generations in the forebrain. We focus our efforts on two nuclei, PAm and DM, which form a critical link in the recurrent song system network. They each receive direct input from the descending motor pathway and projecting bilaterally back to HVC, a key forebrain vocal control nucleus, via the intermediary of the thalamic relay nucleus Uva. We hypothesize that these nuclei play a critical role in synchronizing premotor activity in both hemispheres during key transitions in the song. These experiments are important because Uva lesions completely disrupt song behavior and because of our near complete lack of understanding of the functional role of the vocal-respiratory brainstem in song pattern generation. In the first aim, we propose to characterize neural properties in PAm and DM and evaluate their functional relationship to neurons in their primary input and output structures. We will perform these experiments in restrained sleeping birds. This allows a greater range of experimental accessibility, such as paired recordings. We will use several experimental paradigms, including stimulus-evoked vocalizations and song presentation, that can "drive" the motor system in order to examine network properties under conditions that approach vocal production. In the second aim, we will record from single neurons in both PAm and DM in awake vocalizing birds to gain insight into their firing properties during vocal production. We will carefully quantify the relationship between activity patterns and vocal output. In the final aim, we will investigate the relationship, during vocal production, between input-output networks of neurons in the vocal-respiratory brainstem. We will take advantage of the variability in song output across renditions to inform us about the role of each of these different structures in song pattern generation. Understanding the emerging principles of brainstem-to-forebrain motor signaling and the role the respiratory system might play in vocal control will provide insight into the neural control of complex motor behavior including human speech production and its pathologies

Public Health Relevance

Brainstem respiratory networks are not well integrated within the context of vocal production because they are often viewed exclusively as output structures. In this proposal, we aim to investigate the nature of brainstem-to-forebrain motor signaling and the role the respiratory system plays in vocal control. This work will provide insight into the neural control of complex motor behavior, including human speech production and its pathologies.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC006102-10
Application #
8305048
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Shekim, Lana O
Project Start
2003-03-15
Project End
2014-07-31
Budget Start
2012-08-01
Budget End
2014-07-31
Support Year
10
Fiscal Year
2012
Total Cost
$285,412
Indirect Cost
$102,133
Name
University of Pennsylvania
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
042250712
City
Philadelphia
State
PA
Country
United States
Zip Code
19104
Schmidt, Marc F; Martin Wild, J (2014) The respiratory-vocal system of songbirds: anatomy, physiology, and neural control. Prog Brain Res 212:297-335
McLean, Judith; Bricault, Sarah; Schmidt, Marc F (2013) Characterization of respiratory neurons in the rostral ventrolateral medulla, an area critical for vocal production in songbirds. J Neurophysiol 109:948-57
Maguire, Sarah E; Schmidt, Marc F; White, David J (2013) Social brains in context: lesions targeted to the song control system in female cowbirds affect their social network. PLoS One 8:e63239
Raksin, Jonathan N; Glaze, Christopher M; Smith, Sarah et al. (2012) Linear and nonlinear auditory response properties of interneurons in a high-order avian vocal motor nucleus during wakefulness. J Neurophysiol 107:2185-201
Lewandowski, Brian C; Schmidt, Marc (2011) Short bouts of vocalization induce long-lasting fast ýý oscillations in a sensorimotor nucleus. J Neurosci 31:13936-48
Schmidt, Marc F (2008) Using both sides of your brain: the case for rapid interhemispheric switching. PLoS Biol 6:e269
Ashmore, Robin C; Renk, Jessica A; Schmidt, Marc F (2008) Bottom-up activation of the vocal motor forebrain by the respiratory brainstem. J Neurosci 28:2613-23
Ashmore, Robin C; Bourjaily, Mark; Schmidt, Marc F (2008) Hemispheric coordination is necessary for song production in adult birds: implications for a dual role for forebrain nuclei in vocal motor control. J Neurophysiol 99:373-85
Cardin, Jessica A; Raksin, Jonathan N; Schmidt, Marc F (2005) Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. J Neurophysiol 93:2157-66
Ashmore, Robin C; Wild, J Martin; Schmidt, Marc F (2005) Brainstem and forebrain contributions to the generation of learned motor behaviors for song. J Neurosci 25:8543-54