Spatially and non-spatially tuned hippocampal neurons are linear perceptual and nonlinear memory encoders

Abstract

The hippocampus has long been regarded as a neural map of physical space, with its neurons categorized as spatially or non-spatially tuned according to their response selectivity. However, growing evidence suggests that this dichotomy oversimplifies the complex roles hippocampal neurons play in integrating spatial and non-spatial information. Through computational modeling and in-vivo electrophysiology in macaques, we show that neurons classified as spatially tuned primarily encode linear combinations of immediate behaviorally relevant factors, while those labeled as non-spatially tuned rely on nonlinear mechanisms to integrate temporally distant experiences. Furthermore, our findings reveal a temporal gradient in the primate CA3 region, where spatial selectivity diminishes as neurons encode increasingly distant past events. Finally, using artificial neural networks, we demonstrate that nonlinear recurrent connections are crucial for capturing the response dynamics of non-spatially tuned neurons, particularly those encoding memory-related information. These findings challenge the traditional dichotomy of spatial versus non-spatial representations and instead suggest a continuum of linear and nonlinear computations that underpin hippocampal function. This framework provides new insights into how the hippocampus bridges perception and memory, informing on its role in episodic memory, spatial navigation, and associative learning.