Rats learned, using distal room cues, to run to a goal on an elevated, circular track starting from any position on the track. The goal was one of eight equidistant, recessed cups set around the track, the goal cup being distinguished from the others solely by its position in the room. After learning, electrolytic lesions were made in the medial septal nucleus eliminating hippocampal theta rhythm in some animals but not in others. Rats without theta rhythm were no longer able to perform the spatial task, whereas rats with undisturbed theta rhythm retrained normal performance. Although rats without theta rhythm could not find their way directly to the goal, they recognized its location when they came upon it by chance. This type of spatial deficit appears similar to that shown by hippocampally lesioned patient H.M. Subsequent tests demonstrated that rats deprived of theta rhythm before training could nevertheless learn the task.

Rat hippocampal (CA1) complex spike "place cells" of freely behaving rats were recorded in pairs continuously during a series of waking (exploration and still-alert), drowsy (quiet-awake), and sleeping (slow-wave, pre-rapid-eye-movement and rapid-eye-movement sleep) behaviors. Pairs of units were selected that had nonoverlapping place fields. The rats were restricted from entering the place field of either cell overnight, and on the day of recording cells were exposed to their individual place fields independently and in a counterbalanced manner. Following exposure, recordings were made in the subsequent sleep episodes and the firing characteristics of both cells were analyzed. Following exposure, significant increases in the spiking activity of the exposed cell were observed in the subsequent sleeping states that were not evident in the unexposed cell. The increased activity was observed in the rate of firing (spikes/sec), the rate of occurrence of bursts with multiple spikes, as well as the number of bursts displaying short (2-4 msec) interspike intervals. The findings suggest that neuronal activity of hippocampal place cells in the awake states may influence the firing characteristics of these cells in subsequent sleep episodes. The increased firing rates along with the greater number of multiple spike bursts and the shorter interspike intervals within the burst, following exposure to a cell's place field, may represent possible information processing during sleep.

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1. In chronically prepared, freely moving rats, electrical stimulation was applied to the angular bundle, and responses were recorded extracellularly at a variety of sites in the ipsilateral hippocampal formation. At each recording site the stimulus-response relationship was tested during four different behavioral states. These were slow-wave sleep (SWS), REM sleep ( REM), and also two waking behaviors consisting of the still, alert condition (labeled SAL), and voluntary movement (AW theta). 2. Two varieties of evoked responses were recorded: those due to the synchronous firing of neuronal action potentials (EAPs) and those produced by excitatory synaptic activity (ESPs). The overall pattern of monosynaptic, di-, and trisynaptic responses found was similar in the rat to that found by Andersen et al. (3-5) in cat and rabbit. 3. When the trisynaptic EAP was recorded in CA1, the threshold was similar during all four behavioral states. However, suprathreshold stimuli evoked a greater response during SWS than during the other three states. The trisynaptic ESP was also greater during SWS. 4. Disynaptically, EAPs were recorded in CA3. These were greater in magnitude during SWS than during SAL, but were intermediate in mean amplitude during AWtheta and REM. Response variability was much greater during AWtheta and REM. 5. The monosynaptic EAP recorded in the upper blade of the dentate gyrus (DG) exhibited the same behaviorally correlated properties found disynaptically in CA3. 6. The monosynaptic ESP recorded in the DG, in contrast to the EAP, was greater in magnitude during SAL than during SWS. 7. The primary afferent volley was also recorded at high gain in the DG. The amplitude of this was found to be dependent solely on stimulus intensity and not on behavioral state. 8. The results are interpreted as suggesting that the granule cell membranes in the DG are relatively hyperpolarized during SAL compared with SWS as the result of either tonic excitatory bombardment occurring during SWS or tonic inhibitory bombardment during SAL.

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Electrical stimuli were applied to the angular bundle of the freely moving rat, and the neuronal responses were recorded ipsilaterally in the dentate gyrus and the CA1 field of the hippocampus. The number of neurons responding monosynaptically in the dentate gyrus was relatively small when the animal was alert and not moving but was much greater both during slow-wave sleep and during rapid eye movement sleep. In Ca1, however, the trisynaptic population response was considerably smaller during rapid eye movement sleep and when the animal was alert than during slow-wave sleep. These findings are interpreted in terms of a set of behaviorally dependent "neural gates". Measurement of the synaptic current at the dentate gyrus induced monosynaptically by stimulation of the angular bundle further suggests that the mechanism by which gating occurs at this level is either a tonic inhibitory synaptic influence exerted upon the granule cells during the alert state, a tonic excitatory influence during slow-wave sleep, or both.