Allocentric space is mapped by a widespread brain circuit of functionally specialized cell types located in interconnected subregions of the hippocampal-parahippocampal cortices. Little is known about the neural architectures required to express this variety of firing patterns. In rats, we found that one of the cell types, the grid cell, was abundant not only in medial entorhinal cortex (MEC), where it was first reported, but also in pre- and parasubiculum. The proportion of grid cells in pre- and parasubiculum was comparable to deep layers of MEC. The symmetry of the grid pattern and its relationship to the theta rhythm were weaker, especially in presubiculum. Pre- and parasubicular grid cells intermingled with head-direction cells and border cells, as in deep MEC layers. The characterization of a common pool of space-responsive cells in architecturally diverse subdivisions of parahippocampal cortex constrains the range of mechanisms that might give rise to their unique functional discharge phenotypes.