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The Journal of Neuroscience, March 5, 2008, 28(10):2447-2458; doi:10.1523/JNEUROSCI.1926-07.2008

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Cellular/Molecular
Generation of Eupnea and Sighs by a Spatiochemically Organized Inspiratory Network

Araya Ruangkittisakul,¹ Stephan W. Schwarzacher,² Lucia Secchia,¹ Yonglie Ma,¹ Nicoleta Bobocea,¹ Betty Y. Poon,¹ Gregory D. Funk,¹ and Klaus Ballanyi¹

¹Department of Physiology and Perinatal Research Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2S2, and ²Department of Anatomy and Neuroanatomy, University of Frankfurt, 60590 Frankfurt/Main, Germany

Correspondence should be addressed to Dr. Klaus Ballanyi at the above address. Email: klaus.ballanyi{at}ualberta.ca

The discovery of the rhythmogenic pre-Bötzinger complex (preBötC) inspiratory network, which remains active in a transverse brainstem slice, greatly increased the understanding of neural respiratory control. However, basic questions remain unanswered such as (1) What are the necessary and sufficient slice boundaries for a functional preBötC? (2) Is the minimal preBötC capable of reconfiguring between inspiratory-related patterns (e.g., fictive eupnea and sighs)? (3) How is preBötC activity affected by surrounding structures? Using newborn rat slices with systematically varied dimensions in physiological [K⁺] (3 mM), we found that a 175 µm thickness is sufficient for generating inspiratory-related rhythms. In 700-µm-thick slices with unilaterally exposed preBötC, a kernel <100 µm thick, centered 0.5 mm caudal to the facial nucleus, is necessary for rhythm generation. Slices containing this kernel plus caudal structures produced eupneic bursts of regular amplitude, whereas this kernel plus rostral tissue generated sighs, intermingled with eupneic bursts of variable amplitude ("eupnea–sigh pattern"). After spontaneous arrest of rhythm, substance-P or neurokinin-1 (NK1) receptor agonist induced the eupnea–sigh burst pattern in 250-µm-thick slices, whereas thyrotropin-releasing hormone or phosphodiesterase-4 blockers evoked the eupnea burst pattern. Endogenous rhythm was depressed by NK1 receptor antagonism. Multineuronal Ca²⁺ imaging revealed that preBötC neurons reconfigure between eupnea and eupnea–sigh burst patterns. We hypothesize a (gradient-like) spatiochemical organization of regions adjacent to the preBötC, such that a small preBötC inspiratory-related oscillator generates eupnea under the dominant influence of caudal structures or thyrotropin-releasing hormone-like transmitters but eupnea–sigh activity when the influence of rostral structures or substance-P-like transmitters predominates.

Key words: eupnea; histology; brain stem; pre-Bötzinger; respiratory rhythm; Ca²⁺ imaging

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Received April 27, 2007; revised Jan. 14, 2008; accepted Jan. 15, 2008.

Correspondence should be addressed to Dr. Klaus Ballanyi at the above address. Email: klaus.ballanyi{at}ualberta.ca

This article has been cited by other articles:

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