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J Appl Physiol (December 20, 2002). doi:10.1152/japplphysiol.00639.2002
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Submitted on July 15, 2002
Accepted on November 15, 2002

Integration-Differentiation and Gating of Carotid Afferent Traffic that Shapes the Respiratory Pattern

Daniel L Young1, Frederick L Eldridge2, and Chi-Sang Poon1*

1 Harvard-MIT Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA, USA
2 Department of Cell and Molecular Physiology, University of North Carolina, Chapel Hill, NC, USA

* To whom correspondence should be addressed. E-mail: cpoon{at}mit.edu.

The phase-dependent plasticity of carotid chemoafferent signaling was studied with electrical stimulation of a carotid sinus nerve (CSN) during either inspiration or expiration in anesthetized, glomectomized, vagotomized, paralyzed and ventilated rats. Stroboscopic and interferometric analyses of the resulting phase-contrast disturbances of the respiratory rhythm revealed that carotid chemoafferent traffic was dynamically filtered centrally by a parallel bank of leaky integrators and differentiators, each being logically gated to the inspiratory or expiratory phase in a stop-and-go manner as follows: (1) carotid short-term potentiation of inspiratory drive was mediated by dual integrators that both shortened inspiration and augmented phrenic motor output cooperatively in long and short timescales; (2) carotid short-term depression of respiratory frequency was mediated by a (possibly pontine) integrator that lengthened expiration with a relatively long memory; (3) carotid 'chemoreflex' shortening of expiration was mediated by an occult fast integrator which, together with carotid short-term depression, formed a differentiator. These effects were modulated anteriorly by integrators in the nucleus tractus solitarius that were 'auto-gated' to--or recruited by--the CSN input. Such phase-selective and activity-dependent time-frequency filtering of carotid chemoafferent feedback in parallel neurologic-neurodynamic central pathways may profoundly affect respiratory stability during hypoxia and sleep, and could contribute to the dynamic optimization of respiratory pattern and maintenance of homeostasis in health and in disease states.




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