Experience-dependent place-cell referencing in hippocampal area CA1

Abstract

CA1 hippocampal place cells (PCs) are known for using both self-centric (egocentric) and world-centric (allocentric) reference frames to support a cognitive map1,2. The mechanism of PC referencing and the role of experience in this process, however, remain poorly understood3-5. Here we longitudinally recorded the activity of CA1 PCs while mice performed a spatial learning task. In a familiar environment, the CA1 representation consisted of PCs that were referenced to either spatial locations (allocentric PCs) or mouse running (egocentric PCs) in approximately equal proportions. In a novel environment, however, the CA1 representation became predominately egocentrically referenced. Notably, individual allocentric PCs in a familiar environment adaptively switched reference frames to become egocentric in a novel environment. In addition, intracellular membrane potential recordings revealed that individual CA1 neurons simultaneously received both ego- and allo-centric synaptic inputs, and the ratio of these two input streams correlated with the level of individual PC referencing. Furthermore, behavioral timescale synaptic plasticity6,7 (BTSP) was an active participant in shaping PC referencing through the rapid adjustment of synaptic weights on many PCs. Together, these results suggest that experience-dependent adjustment of synaptic input shapes ego and allocentric PC referencing to support a flexible cognitive map in CA1.