Lateral hypothalamus neuron involvement in integration of natural and artificial rewards and cue signals

Abstract

Involvement of rat lateral hypothalamus (LHA) neurons in integration of motivation, reward, and learning processes was studied by recording single-neuron activity during cuetone discrimination, learning behavior to obtain glucose, or electrical rewarding intracranial self-stimulation (ICSS) of the posterior LHA. To relate the activity of an LHA neuron to glucose, ICSS, and anticipatory cues, the same licking task was used to obtain both rewards. Each neuron was tested with rewards alone and then with rewards signaled by cuetone stimuli (CTS), CTS1+ = 1,200 Hz for glucose, CTS2+ = 4,300 Hz for ICSS, and CTS- = 2,800 Hz for no reward. The activity of 318 neurons in the LHA was analyzed. Of these, 212 (66.7%) responded to one or both rewarding stimuli (glucose, 115; ICSS, 193). Usually, both rewards affected the same neuron in the same direction. Of 96 neurons that responded to both rewards, the responses of 72 (75%) were similar, i.e., either both excitatory or both inhibitory. When a tone was associated with glucose or ICSS reward, 81 of the 212 neurons that responded to either or both rewards and none of 106 neurons that failed to respond to either reward acquired a response to the respective CTS. Usually, the response to a tone was in the same direction as the reward response. Of 45 neurons that responded to both glucose and CTS1+, 38 (84.4%) were similar, and of 66 that responded to both ICSS and CTS2+, 47 (71.2%) were similar. The neural response to a tone was acquired rapidly after licking behavior was learned and was extinguished equally rapidly before licking stopped in extinction. The latency of the neural response to CTS1+ was 10-150 ms (58.7 +/- 40.9 ms, mean +/- SE, n = 31), and that of the first lick was 100-370 ms (204.8 +/- 59.1 ms, n = 31). The latency of neural responses to CTS2+ was 10-230 ms (68.3 +/- 53.5 ms, n = 33), and that of the first lick was 90-370 ms (212.4 +/- 58.5 ms, n = 33). There was no significant difference between the neural response latencies for the two cue tones nor between the lick latencies for the different rewards. Neurons inhibited by glucose or ICSS reward were distributed widely in the LHA, whereas most excited neurons were in the posterodorsal subarea; fewer were in the anteroventral subarea. Neurons responding to the CTS for glucose or ICSS were found more frequently in the posterior region.(ABSTRACT TRUNCATED AT 400 WORDS)