In vivo intracellular correlates of hippocampal formation theta-on and theta-off cells

Abstract

Using urethane-anesthetized rats, intracellular recordings were made in hippocampal formation cells classified according to previously established criteria as either theta-on or theta-off, in order to further define the electrophysiological characteristics of these cells. Four cells classified as phasic theta-off cells had short duration spikes (<1 ms), high input resistances (54–61 MΩ) and large fast afterhyperpolarizations (6–10 mV), thus sharing some of the properties of identified hippocampal interneurons. Phasic theta-off cells also exhibited rhythmic membrane potential oscillations (MPOs) ranging from 4 to 10 mV in amplitude during the simultaneous occurrence of extracellular theta field activity, but not during the occurrence of large amplitude irregular field activity (LIA). The MPOs of phasic theta-off cells were the same frequency as and were highly coherent with the extracellular theta field activity. In all four phasic theta-off cells the positive peak of the MPO was in phase with the positive peak of the local theta field activity. At the onset of extracellular theta field activity above 4–5 Hz, the membrane potentials of phasic theta-off cells showed a 5–10-mV hyperpolarizing shift, accompanied by MPOs without spike discharges. As theta frequency slowed down there was a return to baseline membrane potential levels and spike discharges occurred near the positive peak of the MPOs. The seven cells classified as phasic theta-on had longer duration spikes (>1 ms), lower input resistances (22–36 MΩ) and small (approx. 1.0 mV) fast afterhyperpolarizations, thus sharing some of the properties of hippocampal projection cells. Phasic theta-on cells also exhibited MPOs (4–10 mV) during theta but not during LIA and the MPOs were also the same frequency as and were highly coherent with the extracellular theta field activity. The positive peak of the MPOs were in pahse with the negative peak of the local extracellular theta. At the onset of extracellular theta the membrane potentials of phasic theta-on cells showed a 5–10 mV depolarizing shift accompanied by MPOs and spike discharges occurring near the positive peak of the MPOs. The five tonic theta-on cells and two non-related cells had similar electrophysiological properties as the phasic theta-on cells. Tonic theta-on and non-related cells failed to exhibit MPOs during the occurrence of either extracellular theta field activity or LIA.