Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states.
Using extracellular single unit recording, either alone or in combination with microdialysis application of drugs, we examined the characteristics of presumed serotonergic dorsal raphe neurons during wake-sleep states in the freely moving cat. Recordings were made from a total of 272 neurons in the dorsal raphe nucleus. Of these, 240 (88%) were classified as serotonergic on the basis of their typical long-duration action potential, slow discharge activity, and reduced spontaneous discharge rate during paradoxical sleep compared to during slow-wave sleep. An inhibitory response to serotonergic agonists and a slow conduction velocity were seen in all neurons of this type tested or identified by stimulation of the main ascending serotonergic pathway. These presumed serotonergic dorsal raphe neurons could be subdivided into two typical previously identified groups (types I-A and I-B) and four atypical new groups (types I-C, II-A, II-B, and II-C) according to differences in firing patterns during wake-sleep states. The typical neurons were evenly distributed in the dorsal raphe nucleus and their activity was related to the level of behavioral arousal, since they discharged regularly at a high rate during waking and at progressively slower rates during slow-wave sleep, and ceased firing either during slow-wave sleep with ponto-geniculo-occipital waves and paradoxical sleep (type I-A) or only during paradoxical sleep (type I-B). In contrast, the atypical subgroups were unevenly distributed in the dorsal raphe nucleus and exhibited firing patterns distinct from those of the typical neurons, such as sustained tonic activity during paradoxical sleep (types I-C and II-C) or showing their highest rate of tonic discharge during slow-wave sleep, with suppression of discharge during both waking and paradoxical sleep (type II-B). From these data we suggest that presumed serotonergic dorsal raphe neurons play different roles in behavioral state control and that there is functional topographic organization in the dorsal raphe nucleus.
Sakai
K
K
INSERM U480, Department of Experimental Medicine, Claude Bernard University, Lyon 1, 8 Avenue Rockefeller, 69373 Lyon Cedex 08, France. sakai@univ-lyon1.fr
Crochet
S
S
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000316:Adrenergic alpha-Agonists / Q000494:pharmacology; D000818:Animals; D001522:Behavior, Animal / Q000187:drug effects / Q000502:physiology*; D002415:Cats; D018755:GABA Agonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D006632:Histamine / Q000494:pharmacology; D008636:Mesencephalon / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D017551:Microdialysis; D009434:Neural Pathways / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D009474:Neurons / Q000145:classification / Q000187:drug effects / Q000378:metabolism*; D010507:Periodicity; D011903:Raphe Nuclei / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D012701:Serotonin / Q000378:metabolism*; D012702:Serotonin Antagonists / Q000494:pharmacology; D017366:Serotonin Receptor Agonists / Q000494:pharmacology; D012890:Sleep / Q000187:drug effects / Q000502:physiology*; D012895:Sleep, REM / Q000187:drug effects / Q000502:physiology; D014851:Wakefulness / Q000187:drug effects / Q000502:physiology*
D000316:Adrenergic alpha-Agonists; D018755:GABA Agonists; D018756:GABA Antagonists; D012702:Serotonin Antagonists; D017366:Serotonin Receptor Agonists; D012701:Serotonin; D006632:Histamine