Variable recruitment of distal tuft dendrites shapes new hippocampal place fields

Abstract

SUMMARYHippocampal pyramidal neurons support episodic memory by integrating complementary information streams into new ‘place fields’. Distal tuft dendrites are widely thought to initiate place field formation by locally generating prolonged, globally-spreadingCa2+spikes known as plateau potentials. However, the hitherto experimental inaccessibility of distal tuft dendrites in the hippocampus has rendered theirin vivofunction entirely unknown. Here we gained direct optical access to this elusive dendritic compartment. We report that distal tuft dendrites do not serve as the point of origin for place field-forming plateau potentials. Instead, the timing and extent of peri-formation distal tuft recruitment is variable and closely predicts multiple properties of resultant place fields. Therefore, distal tuft dendrites play a more powerful role in hippocampal feature selectivity than simply initiating place field formation. Moreover, place field formation is not accompanied by globalCa2+influx as previously thought. In addition to shaping new somatic place fields, distal tuft dendrites possess their own local place fields. Tuft place fields are back-shifted relative to that of their soma and appear to maintain somatic place fields via post-formation plateau potentials. Through directin vivoobservation, we provide a revised dendritic basis for hippocampal feature selectivity during navigational learning.