Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethan-anesthetized rat

Abstract

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).(ABSTRACT TRUNCATED AT 400 WORDS)

Evidence for Differential Control of Posterior Hypothalamic, Supramammillary, and Medial Mammillary Theta-Related Cellular Discharge by Ascending and Descending Pathways

“…It seems likely, therefore, that, as has been suggested previously, rhythmical activity in SuM is not necessary for the expression of per se (Kirk and McNaughton, 1993;Bland et al, 1995;Thinschmidt et al, 1995). Further, it has been demonstrated that lesions of the RPO produced little obvious change in hippocampal in freely moving animals (Farris and Sainsbury, 1990).…”

“…It has been suggested McNaughton, 1991, 1993) that the level of ascending tonic RPO input is transduced into the frequency of in the SuM (reflected in the frequency of SuM cell burst discharge), and that this frequency-coded information is then fed via the medial forebrain bundle (Veazy et al, 1982;Vertes, 1992) to the MS/vDBB. The PH, however, may provide tonic input (possibly cholinergic; see Brazhnik and Vinogradova, 1986;Oddie et al, 1994;Bland et al, 1995) to the MS/vDBB and hippocampus that accentuates rhythmic firing in septal cells (Brazhnik and Vinogradova, 1986;Bland et al, 1994) and is required for the expression of field activity in the hippocampus .…”

“…Lesions of, or procaine infused into the region of, the posterior hypothalamus (PH) abolish hippocampal or septal activity (Kawamura et al, 1961;Anchel and Lindsley, 1972;Robinson and Whishaw, 1974;Bland et al, 1994Bland et al, , 1995Oddie et al, 1994), and high-frequency (100 Hz) stimulation in the PH has been shown to be particularly effective in eliciting hippocampal field activity (Bland and Vanderwolf, 1972) and pattern discharge in medial septal cells (Bland et al, 1990). Thus, the PH has also been proposed to be a relay in the ascending synchronizing system.…”

“…Neurons in the mammillary nuclei have also been shown to discharge rhythmically at frequencies (Mignard et al, 1987;Kocsis and Vertes, 1994;Bland et al, 1995), and repetitive bursts have been recorded in vitro from the medial (MM) or lateral (LM) mammillary nucleus Llinás and Alonso, 1992). As with hippocampal , this activity in the mammillary nuclei may subserve their proposed role in memory in general (Mair et al, 1979), and spatial memory in particular (Sziklas and Petrides, 1993).…”

Descending projections of the posterior nucleus of the hypothalamus:Phaseolus vulgaris leucoagglutinin analysis in the rat

“…The posterior hypothalamic nucleus has been linked to several functions including cardiovascular activity, respiration, locomotion, wakefulnessiarousal, antinociception, and recently the modulation of the hippocampal EEG (Shik and Orlovsky, 1976;Buccafusco and Brezenoff, 1979;Eldridge et al, 1981Eldridge et al, , 1985Carstens, 1982;Ohta et al, 1985;DiMicco et al, 1986;DiMicco and Abshire, 1987;Mori, 1987;Martin et al, 1988;Waldrop et al, 1988;Wible et al, 1988;Lin et al, 1989;Pare et al, 1989;Spencer et al, 1990;Sinnamon, 1993;Bland et al, , 1995Vertes et al, 1995). The PH has been viewed as an important center for the integration of these various activities.…”