Hypothalamic neuron involvement in integration of reward, aversion, and cue signals.

Abstract

The lateral hypothalamus (LHA) is involved in integrative functions related to emotion, reward, aversion, and learning. It is, however, unclear whether the medial forebrain bundle (MFB) forms a substrate common to the anterior and posterior hypothalamic areas or whether information regarding rewarding and aversive stimuli converges on and is integrated by the same hypothalamic neuron. In the present study, unit activity in the LHA and lateral preoptic-anterior hypothalamic area (lPOA-AHA) of the rat was recorded during discrimination learning of cue tone stimuli (CTS) that predicted glucose or intracranial self-stimulation (ICSS) as rewarding stimuli, or electric shock or tail pinch as aversive stimuli, using identical behavior, licking. We examined functional differences between the LHA and lPOA-AHA. In positive reinforcement experiments a rat was rewarded by glucose or ICSS only when it licked a spout presented in front of its mouth. The threshold current for ICSS was used. In negative reinforcement experiments an aversive stimulus, either electric shock or tail pinch was applied if the rat did not lick the spout. The strengths of electric shock and tail pinch were selected to produce an avoidance ratio less than 20-30%, averaged in all trials. The activity of 507 LHA and 249 lPOA-AHA neurons was analyzed during both glucose and ICSS trials. The effects of both glucose and ICSS on the same LHA or lPOA-AHA neuron were usually in the same direction, i.e., either both excitatory or both inhibitory. Of 143 LHA and 44 lPOA-AHA neurons that responded to both rewards, the responses of 117 (81.8%) LHA and 35 (79.5%) lPOA-AHA neurons to both stimuli were similar. The activity of 131 LHA and 153 lPOA-AHA neurons was analyzed in both electric shock and tail pinch trials. The effects of both electric shock and tail pinch on the same LHA or lPOA-AHA neuron were usually in the same direction. Of 29 LHA and 27 lPOA-AHA neurons that responded to both aversive stimuli, the responses of 28 (96.6%) LHA and 25 (92.6%) lPOA-AHA neurons to both were similar. The activity of 170 LHA and 195 lPOA-AHA neurons in response to both rewarding glucose and/or ICSS stimulation and aversive electric shock and/or tail pinch was analyzed. About one-third of the neurons in each area were reward specific (57/170 in LHA; 63/195 in lPOA-AHA), whereas relatively few were aversion specific in each area (21/170 in LHA; 15/195 in lPOA-AHA).(ABSTRACT TRUNCATED AT 400 WORDS)