DISCHARGE PATTERNS OF HIPPOCAMPAL THETA-RELATED CELLS IN THE CAUDAL DIENCEPHALON OF THE URETHANE-ANESTHETIZED RAT

1. Single-unit discharge patterns of cells in specific nuclei of the caudal diencephalon were characterized in relation to simultaneously recorded field activity from the stratum moleculare of the dentate gyrus according to the criteria that have been used previously to classify cells in the hippocampal formation (including entorhinal cortex), medial septum, and cingulate cortex. Theta (theta)-related cells were classified as 1) tonic theta-ON, if they discharged nonrhythmically and increased their discharge rates during hippocampal theta relative to large, irregular hippocampal field activity (LIA); 2) tonic theta-OFF, if they discharged nonrhythmically and decreased their discharge rates during theta relative to LIA; or 3) phasic theta-ON, if they discharged rhythmically and in phase with ongoing theta, but nonrhythmically during LIA. Cells not meeting any of the above criteria were classified as nonrelated. 2. Recordings were obtained in a total of 127 cells from the caudal diencephalon. Recordings were made in 54 cells from the posterior hypothalamic nucleus (PH), 16 from the supramammillary nucleus (SuM), 20 from the PH/SuM border, and 23 from the medial mammillary nucleus (MM). Recordings were also made from nine cells from the central medial nucleus of the thalamus (CM) and five from the dorsomedial hypothalamic nucleus (DMH). 3. Of the 54 PH cells, 43 (80%) were classified as tonic theta-ON and 11 (20%) as nonrelated. Tonic theta-ON cells in the PH discharged at significantly higher rates during theta, either occurring spontaneously (9.6 +/- 1.7 Hz, mean +/- SE) or elicited with a tail pinch (TP theta; 10.6 +/- 1.9 Hz), than during LIA (3.6 +/- 1.4 Hz). Of the nine CM cells, seven (78%) were tonic theta-ON and two (22%) were nonrelated. Tonic theta-ON cells discharged at significantly higher rates during theta (17.5 +/- 7.8 Hz) or TP theta (18.0 +/- 7.1 Hz) than during LIA (7.3 +/- 4.8 Hz). All DMH cells were nonrelated. 4. Of the 20 PH/SuM border cells, 15 (75%) were classified as tonic theta-OFF and discharged at significantly higher rates during LIA (5.3 +/- 1.5 Hz) than during theta (0.8 +/- 0.4 Hz) or TP theta (0.4 +/- 0.3 Hz). Five (25%) cells in the PH/SuM border were nonrelated. 5. All of the 16 cells (100%) recorded from the body of the SuM were phasic theta-ON. The discharge rates of these cells did not change significantly across hippocampal field states (LIA = 8.3 +/- 1.6; theta = 7.3 +/- 1.6; TP theta = 8.6 +/- 1.7 Hz). However, all of these cells changed from a nonrhythmic discharge pattern during LIA to a rhythmic (or phasic) discharge pattern during theta. Most of the SuM cells (12 of 16, 75%) discharged on the negativegoing phase of the hippocampal theta recorded from the fissure/stratum moleculare of the dentate gyrus (151 +/- 14 degrees; 0 degrees = positive peak of theta). 6. Of the 23 cells recorded from the MM, 19 (83%) were also phasic theta-ON. The remaining four cells (17%) were nonrelated. The discharge rates of MM phasic theta-ON cells did not change significantly across hippocampal field states (LIA = 9.1 +/- 2.0; theta = 9.9 +/- 1.5; TP theta = 9.4 +/- 1.4 Hz). However, all of these cells changed from a nonrhythmic discharge pattern during LIA. to a rhythmic (or phasic) discharge pattern during theta. In contrast to SuM phasic theta-ON cells, most of the MM cells (15 of 19, 75%) discharged on the positive-going phase of theta (300 +/- 12 degrees). 7. On the basis of these and previously published data, it is suggested that tonic theta-ON cells in the PH (and possibly CM) act in synergy with phasic theta-ON cells in the SuM during hippocampal theta to relay ascending reticular input to the septum. MM cells may, as has previously been suggested, act to relay theta-rhythmic signals from the septum or hippocampus to other parts of the limbic system. It is suggested that tonic theta-OFF cells in the PH/SuM border inhibit discharge of theta-ON cells in the PH and SuM during non-theta hippocampal states.