Responses of lateral hypothalamic glucose-sensitive and glucose- insensitive neurons to chemical stimuli in behaving rhesus monkeys

Z. Karadi, Y. Oomura, H. Nishino, T. R. Scott, L. Lenard, S. Aou

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Abstract

1. Extracellular single neuron activity was recorded in the lateral hypothalamic area (LHA) of awake, behaving monkeys, with particular regard to the feeding-related functional characteristics of glucose-sensitive (GS) versus glucose-insensitive (GIS) neurons. Firing rate changes were recorded by means of carbon fiber, multibarreled glass microelectrodes during 1) microelectrophoretic application of various chemicals, 2) gustatory and olfactory stimulation, and 3) a high fixed-ratio schedule (FR) bar press feeding task. 2. In 336 neurons examined, 91 (27%) were suppressed by electrophoretically administered glucose, and so they were designated as GS cells. The 245 neurons (73%) in which the firing rates did not change during glucose applications were pronounced GIS. The 179 GS and GIS cells tested exhibited different responses to the catecholamines (CAs), noradrenaline (NA) and dopamine (DA), both of which are intimately involved in the control of feeding. More GS neurons responded to NA than did GIS cells; the predominant effect of both CAs on GS neurons was inhibition. 3. The taste responsiveness of 111 LHA neurons was examined. Fifty-seven cells (52%) showed responses to gustatory stimulation. Of 50 GS neurons tested, 33 (66%) exhibited firing rate changes to tastes. On the contrary, only 24 (39%) of the 61 GIS neurons examined responded to gustatory stimuli. Activity changes of GS neurons commonly occurred to two or more tastants, in distinction to the relative gustatory specificity shown by GIS cells. 4. Two hundred fifty-six (84%) of the 303 neurons tested responded during one or more phases of the bar press feeding task. Most activity changes occurred during the bar press (BP) and reward (RW) periods, however numerous phasic responses to cue light (CL) and cue tone (CT) were also observed. A higher proportion of the GS neurons showed task-related activity changes than did the GIS cells (77, 95% and 179, 81%, respectively). GS neurons responded more during the BP phase and to the food reward; GIS cells were more responsive during the CL that enabled acquisition and the CT that signaled reward. Thus GS neurons were responsive during the acquisition and consumption of reward, whereas GIS cells responded to external cues signaling both of these events. The gustatory neurons displayed specific task-related activity changes only in the CL (GIS cells) and BP phases (GS neurons), that is, in phases most intimately involved in sensory-motor integration. 5. Two-thirds of the 30 GS neurons tested were responsive to both gustatory and olfactory stimulation as opposed to only one-third of GIS cells. Twenty-eight of 30 GS neurons (93%) examined through both chemical senses showed responses to at least one of the two modalities. By contrast, 19 of 28 GIS cells (68%) displayed similar activity. 6. Taste- responsive GS and GIS neurons exhibited characteristic differences in their sensitivity to CAs. GS cells were specifically sensitive to NA and gave more inhibitory responses than GIS neurons. Taste-responsive GIS neurons were especially sensitive to DA and responded mainly with excitation. 7. Histological localization of the recording sites revealed a topographical organization of taste-responsive GS and GIS neurons. The former were found more medially and ventrally, whereas the latter were localized along a more dorsolateral axis within the LHA. 8. The two sets of LHA cells appear to have distinct functional roles in processing exogenous and endogenous chemical signals and in the acquisition and reinforcement associated with feeding. GS neurons monitor the internal milieu and utilize associative connections to integrate multimodal chemosensory information. GIS cells are especially sensitive to changes in the external environment, receive specific gustatory and olfactory cues, and so may be important in discriminative mechanisms of the feeding control.

Original languageEnglish
Pages (from-to)389-400
Number of pages12
JournalJournal of Neurophysiology
Volume67
Issue number2
DOIs
Publication statusPublished - Jan 1 1992

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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