Dickson CT, Kirk IJ, Oddie SD, Bland BH
Single-unit discharge patterns of entorhinal cortex (EC) cells were characterized in relation to simultaneously recorded hippocampal (HPC) field activity according to criteria used previously to classify cells in the hippocampal formation, medial septum, cingulate cortex, and caudal diencephalon. EC cells related to HPC theta field activity were classified as 1) phasic theta-on, if they discharged rhythmically, and in phase, with ongoing HPC theta, but nonrhythmically during large, irregular hippocampal field activity (LIA); 2) tonic theta-on, if they discharged nonrhythmically and increased their discharge rates during HPC theta relative to LIA; 3) phasic theta-off, if they discharged rhythmically, and in phase, with ongoing HPC theta, but increased their discharge rates during LIA; and 4) tonic theta-off, if they discharged nonrhythmically and decreased their discharge rates during HPC theta relative to LIA. Cells not meeting any of these criteria were classified as nonrelated. A total of 168 EC cells were recorded, and of these 56 (33%) were classified as theta related, with the remaining 112 (67%) classified as nonrelated. Of the 56 theta-related cells, 41 (73%) had significantly higher discharge rates during HPC theta than during LIA and were classified as theta-on cells (15 phasic theta-on cells and 26 tonic theta-on cells). Nine of the 26 tonic theta-on cells showed a phase relation of their arrhythmic discharges to simultaneously recorded HPC theta field activity. EC phasic theta-on cells did not discharge preferentially on any portion of the HPC theta field recorded from the region of the stratum moleculare of the dentate gyrus. In general, cells classified as phasic revealed a wide distribution of phase preferences. The remaining 15 (26.7%) cells were classified as theta-off cells and discharged at higher rates during HPC LIA than during HPC theta field activity (3 phasic theta-off cells and 12 tonic theta-off cells). Systemic administration of physostigmine significantly increased the discharge rate of tonic and phasic theta-on cells relative to LIA. Electrical stimulation in the posterior hypothalamic region (PH) significantly increased the discharge rate of EC theta-on cells and significantly decreased the discharge rate of EC theta-off cells relative to HPC LIA. The discharge rates of nonrelated EC cells were not influenced by electrical stimulation of the PH. Procaine microinfusion into the medical septum (MS) abolished spontaneously occurring HPC theta and theta induced with PH stimulation. In addition, 5 min after MS procaine, the ability of PH stimulation to modulate EC theta-on cell discharge was abolished. The modulation of cellular discharges produced by PH stimulation recovered by 60 min post-procaine infusion into the MS. The findings support two main conclusions: 1) theta-related cells in the EC are comprised of two main populations of cells, theta-on and theta-off, similar to other regions of limbic cortex and nuclei of the ascending brainstem synchronizing pathway; 2) the ascending brainstem synchronizing pathway exerts both similar and parallel effects on theta-related cells in entorhinal cortex and hippocampus.