State-dependent circuit dynamics of superficial and deep CA1 pyramidal cells in macaques

Diverse neuron classes in hippocampal CA1 have been identified through their heterogeneity in cellular/molecular composition. How these classes relate to the hippocampal function and network dynamics that support cognition in primates remains unclear. Here we report functional cell groups in CA1 of freely-behaving macaques that show a range of spectral phase preferences and varied responses to local network states like the sharp-wave ripple. Segregating superficial- from deep-layer pyramidal cells uncovered differences in firing rate, burstiness, and sharp-wave ripple associated firing. They also showed strata-specific interactions with the inhibitory cell groups. CA1 ensemble recordings revealed the first observations of cell assemblies in the macaque hippocampus, and show that the stratification of pyramidal cells in primates is a major organizing principle of assemblies. These results suggest a sublayer-specific circuit organization in hippocampal CA1 of the freely-behaving macaque that may support dissociable contributions across cognitive and behavioral processes in the primate.