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The Journal of Neuroscience, May 3, 2006, 26(18):4860-4869; doi:10.1523/JNEUROSCI.4607-05.2006

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Behavioral/Systems/Cognitive
A Mechanism for Vocal-Respiratory Coupling in the Mammalian Parabrachial Nucleus

Michael Smotherman,^1,3 Kohta Kobayasi,¹ Jie Ma,¹ Shuyi Zhang,^4,5 and Walter Metzner^1,2

¹Department of Physiological Science and ²Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095, ³Department of Biology, Texas A&M University, College Station, Texas 77845-3258, ⁴Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, China, and ⁵Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou 510663, China

Correspondence should be addressed to Michael Smotherman, Texas A&M University, Biology Department, 3258 TAMU, College Station, TX 77845-3258. E-mail: Email: smotherman{at}tamu.edu

Mammalian vocalizations require the precise coordination of separate laryngeal and respiratory motor pathways. Precisely how and where in the brain vocal motor patterns interact with respiratory rhythm control is unknown. The parabrachial nucleus (PB) is known to mediate key respiratory reflexes and is also considered a principle component of the mammalian vocal motor pathway, making it a likely site for vocal-respiratory interactions, yet a specific role for the PB in vocalizing has yet to be demonstrated. To investigate the role of the PB in vocal-respiratory coordination, we pharmacologically manipulated synaptic activity in the PB while spontaneously vocalizing horseshoe bats were provoked to emit either short, single syllable or long, multisyllabic vocal motor patterns. Iontophoresis of the GABA_A agonist muscimol (MUS) into the lateral PB extended expiratory durations surrounding all vocalizations and increased mean call durations. Alternatively, application of the GABA_A antagonist bicuculline methiodide (BIC) shortened expirations and call durations. In addition, BIC eliminated the occurrence of multisyllabic vocalizations. BIC caused a mild increase in quiet breathing rates, whereas MUS tended to slow quiet breathing. The results indicate that GABA_A receptor-mediated inhibition in the lateral PB modulates the time course of respiratory phase switching during vocalizing, and is needed for proper coordination of calling and breathing in mammals. We hypothesize that vocal-respiratory rhythm entrainment is achieved at least in part via mechanisms similar to other forms of locomotor-respiratory coupling, namely somatosensory feedback influences on respiratory phase-switching in the lateral PB.

Key words: respiration; vocalization; echolocation; sensorimotor; parabrachial; speech

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Received Oct. 27, 2005; revised March 28, 2006; accepted March 29, 2006.

Correspondence should be addressed to Michael Smotherman, Texas A&M University, Biology Department, 3258 TAMU, College Station, TX 77845-3258. E-mail: Email: smotherman{at}tamu.edu

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