Gradual evolution of multiplexed spatial coding within a conserved hippocampal scaffold

The hippocampus constructs spatial maps for navigation, yet their format differs markedly across species. Whether divergences reflect ecological adaptation, phylogenetic architecture, or flexible coding strategy within a conserved circuit has been difficult to disentangle. We recorded CA1 in rats and tree shrews (Tupaia belangeri chinensis), a mammal phylogenetically and ecologically between rodents and primates, using identical tasks and analyses. Unlike the position-dominant code of rats, tree shrew CA1 exhibited a hybrid representation: weaker position selectivity, stronger non-positional tuning, and prevalent multiplexing approaching primate characteristics. Multiplexed populations decoded location as accurately as rat position populations while using fewer neurons, suggesting computational advantages of high-dimensional coding. Despite this representational shift, proximo-distal gradient, pattern completion, and global remapping persisted. Representational format can be tuned without altering the underlying circuit. Tree shrews occupy an evolutionary intermediate in which ancestral network dynamics are repurposed for efficient multiplexed coding, tracing a transition toward primate-like spatial representations.