Rat exploratory behavior controlled by intracranial self-stimulation improves the study of place cell activity

This report is limited to the description of a procedure that should help to resolve the question whether firing fields of hippocampal place cells are relatively stable or modifiable by learning. Rats implanted with lateral hypothalamic electrodes for rewarding intracranial self-stimulation (ICSS) were trained to explore a circular open field (100 cm in diameter) while their locomotion was tracked by a computerized video system which also delivers ICSS whenever the animal's exploration has met certain experimenter defined criteria. The 3 following conditions were examined. (1) Homogeneous exploration of the entire field: ICSS was delivered after the animal repeatedly visited 5 equal segments of the field (central annulus and remainders of the 4 quadrants), entered randomly located circular areas of the field, and/or traveled a criterion distance. (2) Place field contingent reward or non-reward: ICSS was delivered when the animal entered a circular area (23 cm in diameter) corresponding to the place field after a previous visit to a similar area outside the place field. These conditions were reversed in the following task. (3) Delayed reward: ICSS was delivered when the animal entered the circular area and remained in it for 2 s. Each condition was tested for 600 s or until 50 ICSS were delivered. The behavioral procedures described make it possible to propose an experimental protocol that allows examination of the same place cell under conditions of homogeneous exploration with a segment condition or randomly distributed reward and under conditions with the place field signaling reward or non-reward. The delayed reward condition increases the accuracy of the target location and allows assessment of the phasic versus tonic nature of the place cell firing.