Theta- and movement velocity-related firing of hippocampal neurons is disrupted by lesions centered on the perirhinal cortex

The hippocampus is critically involved in spatial memory and navigation. It has previously been proposed that, as part of this process, the hippocampus might have access to self-motion information. The possibility that some of this information may originate from the perirhinal cortex, a region involved in high-order multimodal processing, was tested in the present study by recording the responses of hippocampal complex-spike (place cells) and theta cells (putative interneurons) to movement velocity and to the movement-related theta rhythm EEG while rats with bilateral ibotenic acid lesions centered on the perirhinal cortex (n = 5), or control surgeries (n = 5), foraged in a rectangular environment. Perirhinal cortex lesions altered several characteristics of place and theta cell firing. First, the proportion of theta cells recorded was significantly lower in perirhinal lesion animals (8/39 units) compared to controls (22/53 units). Second, the firing of place cells recorded from lesion animals was phase-shifted so as to occur significantly earlier during the theta rhythm cycle than in place cells from controls (mean difference = 48.73degrees). Third, the firing rates of a significantly lower proportion of place cells from lesion animals were modulated by the movement velocity of the animal compared to place cells from controls. These results indicate that the perirhinal cortex contributes to the responses of hippocampal CA1 place cells by providing information about self-movement and by controlling the timing of firing of these cells. This information may normally be utilized by the hippocampus during spatial memory and navigation processes. Hippocampus 2003;13:93-108. (C) 2003 Wiley-Liss, Inc.