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This Article Full Text Full Text (PDF) All Versions of this Article: 102/3/1577    most recent 00381.2009v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Google Scholar Articles by Erlichman, J. S. Articles by Leiter, J. C. PubMed PubMed Citation Articles by Erlichman, J. S. Articles by Leiter, J. C.

Chemosensory Responses to CO₂ in Multiple Brain Stem Nuclei Determined Using a Voltage-Sensitive Dye in Brain Slices From Rats

¹Department of Biology, St. Lawrence University, Canton, New York; ²Department of Anatomy and Physiology, Wright State Medical School, Dayton, Ohio; and ³Department of Physiology, Dartmouth Medical School, Lebanon, New Hampshire

Submitted 1 May 2009; accepted in final form 18 June 2009

Abstract

We used epifluorescence microscopy and a voltage-sensitive dye, di-8-ANEPPS, to study changes in membrane potential during hypercapnia with or without synaptic blockade in chemosensory brain stem nuclei: the locus coeruleus (LC), the nucleus of the solitary tract, lateral paragigantocellularis nucleus, raphé pallidus, and raphé obscurus and, in putative nonchemosensitive nuclei, the gigantocellularis reticular nucleus and the spinotrigeminal nucleus. We studied the response to hypercapnia in LC cells to evaluate the performance characteristics of the voltage-sensitive dye. Hypercapnia depolarized many LC cells and the voltage responses to hypercapnia were diminished, but not eradicated, by synaptic blockade (there were intrinsically CO₂-sensitive cells in the LC). The voltage response to hypercapnia was substantially diminished after inhibiting fast Na⁺ channels with tetrodotoxin. Thus action potential–related activity was responsible for most of the optical signal that we detected. We systematically examined CO₂ sensitivity among cells in brain stem nuclei to test the hypothesis that CO₂ sensitivity is a ubiquitous phenomenon, not restricted to nominally CO₂ chemosensory nuclei. We found intrinsically CO₂ sensitive neurons in all the nuclei that we examined; even the nonchemosensory nuclei had small numbers of intrinsically CO₂ sensitive neurons. However, synaptic blockade significantly altered the distribution of CO₂-sensitive cells in all of the nuclei so that the cellular response to CO₂ in more intact preparations may be difficult to predict based on studies of intrinsic neuronal activity. Thus CO₂-sensitive neurons are widely distributed in chemosensory and nonchemosensory nuclei and CO₂ sensitivity is dependent on inhibitory and excitatory synaptic activity even within brain slices. Neuronal CO₂ sensitivity important for the behavioral response to CO₂ in intact animals will thus be determined as much by synaptic mechanisms and patterns of connectivity throughout the brain as by intrinsic CO₂ sensitivity.