Sensory responsiveness of "broad-spike" neurons in the laterodorsal tegmental nucleus, locus coeruleus and dorsal raphe of awake rats: implications for cholinergic and monoaminergic neuron-specific responses

Neuroscience. 1994 Dec;63(4):1021-31. doi: 10.1016/0306-4522(94)90569-x.

Abstract

Although cholinergic neurons in the laterodorsal and pedunculopontine tegmental nuclei have been shown to have a pivotal role in neural mechanisms of paradoxical sleep, their function during wakefulness is less understood. To examine the latter, we have recorded from "broad-spike neurons", which were distinguished by their long spike duration, in the laterodorsal tegmental nucleus of undrugged, head-restrained rats, and examined their response properties to sensory stimuli such as light touch to the tail, air puff to the face, 2 kHz pure tone and flashes of light. Broad-spike neurons from the locus coeruleus and dorsal raphe nucleus were studied for comparison; these neurons have been demonstrated to be noradrenergic and serotonergic, respectively. The broad-spike neurons in the laterodorsal tegmental nucleus have also been suggested to be cholinergic. There were two kinds of responses: (1) a simple increase or decrease in firing, reflecting an elevated level of vigilance; and (2) a phasic response composed of a single spike or brief, high frequency burst, usually diminishing or disappearing upon repetition of the stimulus. When two or more types of stimuli were effective in a neuron, they evoked responses of the same quality. Most of the dorsal raphe neurons displayed only the simple increase of firing, whereas the locus coeruleus neurons gave a phasic response with rather weak attenuation upon repetition. Compared with these, the laterodorsal tegmental neurons were heterogeneous: about one-quarter showing only a simple change of firing (half increasing, half decreasing); and two-thirds displaying phasic responses. The latter response of many neurons attenuated strongly upon repetition. The laterodorsal tegmental neurons were classified into several groups according to their spontaneous firing behavior during sleep and wakefulness, but every neuron in a group did not show the same type of response. For example, some of the neurons which were most active during paradoxical sleep and essentially silent during wakefulness decreased or stopped firing upon sensory stimulation, while others in this group had strong phasic responses. These results suggest that putative cholinergic neurons in the laterodorsal tegmental nucleus have heterogenous properties not only with respect to their spontaneous activity during sleep and wakefulness but also with respect to their response to sensory stimulation. Some of these neurons may function to induce a global attentive state in response to a novel stimulus.

MeSH terms

  • Acoustic Stimulation
  • Action Potentials / physiology
  • Animals
  • Biogenic Monoamines / physiology*
  • Brain / cytology
  • Brain / physiology*
  • Electroencephalography
  • Electromyography
  • Locus Coeruleus / cytology
  • Locus Coeruleus / physiology
  • Male
  • Neurons, Afferent / physiology*
  • Norepinephrine / physiology
  • Parasympathetic Nervous System / physiology*
  • Photic Stimulation
  • Physical Stimulation
  • Raphe Nuclei / cytology
  • Raphe Nuclei / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Serotonin / physiology
  • Tegmentum Mesencephali / cytology
  • Tegmentum Mesencephali / physiology

Substances

  • Biogenic Monoamines
  • Serotonin
  • Norepinephrine