How visual scenes recruit spatial maps: threshold-gated activation in CA3 versus continuous integration in CA1

The hippocampal cognitive map is constructed from environmental sensory inputs, but the conditions that recruit a spatial map from a quiescent baseline remain unclear. Using a parametric virtual reality paradigm with simultaneous recordings from CA1 and CA3 in rats, we demonstrate that these subregions follow fundamentally different rules. CA1 place cells exhibited robust selectivity under sparse conditions, continuously updating their tuning as landmarks accumulated. Conversely, CA3 remained quiescent, its recruitment nonlinearly gated until landmarks formed a spatiotemporally integrated ensemble, governed by ensemble density and configuration rather than absolute count. Naturalistic backgrounds facilitated early activation, eliciting stepwise recruitment as scene complexity increased. These transitions paralleled LFP dynamics shifting from sensory decoupling (reduced fast-gamma coupling) to global network engagement (increased slow-gamma coupling). Together, these findings establish a circuit-level framework wherein CA3 operates as a nonlinearly gated scene constructor and CA1 as a continuous landmark integrator to build and maintain the cognitive map.