Complementary spatial firing in place cell-interneuron pairs

The hippocampal formation plays a pivotal role in representing the physical environment. While CA1 pyramidal cells display sharply tuned location-specific firing, the activity of many interneurons show weaker but significant spatial modulation. Although hippocampal interneurons were proposed to participate in the representation of space, their interplay with pyramidal cells in formation of spatial maps is not well understood. In this study, we investigated the spatial correlation between CA1 pyramidal cells and putative interneurons recorded concurrently in awake rats. Positively and negatively correlated pairs were found to be simultaneously present in the CA1 region. While pyramidal cell-interneuron pairs with positive spatial correlation showed similar firing maps, negative spatial correlation was often accompanied by complementary place maps, which could occur even in the presence of a monosynaptic excitation between the cells. Thus, location-specific firing increase of hippocampal interneurons is not necessarily a simple product of excitation by a pyramidal cell with a similarly positioned firing field. Based on our observation of pyramidal cells firing selectively in the low firing regions of interneurons, we speculate that the location-specific firing of place cells is partly determined by the location-specific decrease of interneuron activity that can release place cells from inhibition.The hippocampus plays a pivotal role in spatial navigation as hippocampal pyramidal cells display sharply tuned location-specific firing (firing/place fields). Recent studies have established that hippocampal interneurons have also well-defined place fields, with important implications for spatial navigation. However, it remains to be determined whether the shape of interneuron place fields is critically dependent on the firing patterns of pyramidal cells or vice versa. We show that pyramidal cell-interneuron pairs with similar and complementary spatial firing are simultaneously present in the rat hippocampus, and the latter occurs even in the presence of a positive temporal correlation in firing. Based on our observation we argue that interneuron place fields are not a simple product of their spatially tuned pyramidal cell inputs and speculate that the location-specific firing of place cells is at least partly determined by the location-specific decrease of interneuron activity that can release place cells from inhibition. © 2010 The Authors. Journal compilation © 2010 The Physiological Society.