Distributed neural codes of the 3D position in the marmoset frontal cortex and hippocampus

The neural encoding of the animal's position is essential for spatial navigation and cognition, yet the three-dimensional (3D) positioning system in the primate brain remains poorly understood. By combining wireless multi-channel recordings from common marmosets with a free-forging task in the 3D space, we identified 42% and 24% neurons in the frontal cortex (FC) and hippocampus (HPC) as place cells, respectively. Place cells in FC and HPC encoded the 3D position with similar spatial information, sparsity and stability, and exhibited stronger functional connections than non-place cells. Notably, their place fields were preferentially distributed in the center and border of the 3D space, and were recapitulated by an RNN-AutoEncoder model simulating the FC-HPC network. Collectively, these findings support a hypothesis that a widely distributed neural network involving frontal cortex and hippocampus constitutes a 3D positioning system in primates possibly by local recurrent circuits and long-range connections.