TASK-DEPENDENT REPRESENTATIONS IN RAT HIPPOCAMPAL PLACE NEURONS

It is suggested that the hippocampal formation is essential to spatial representations by flexible encoding of diverse information during na vigation, which includes not only externally generated sensory informa tion such as visual and auditory sensation but also ideothetic informa tion concerning locomotion (i.e., internally generated information suc h as proprioceptive and vestibular sensation) as well as information c oncerning reward. In the present study, we investigated how various ty pes of information are represented in the hippocampal formation, by re cording hippocampal complex-spike cells from rats that performed three types of place learning tasks in a circular open field with the use o f intracranial self-stimulation as reward. The intracranial self-stimu lation reward was delivered in the following three contexts: if the ra t 1) entered an experimenter-determined reward place within the open f ield, and this place was randomly varied in sequential trials; 2) ente red two specific places, one within and one outside the place field (a n area identified by change in activity of a place neuron); or 3) ente red an experimenter-specified place outside the place field. Because t he behavioral trails during navigation were more constant in the secon d task than in the first task, ideothetic information concerning locom otion was more relevant to acquiring reward in the second task than in the first task. Of 43 complex-spike cells recorded, 37 displayed plac e fields under the first task. Of these 37 place neurons, 34 also had significant reward correlates only inside the place field. Although re ward and place correlates of the place neuron activity did not change between the first and second tasks, neuronal correlates to behavioral variables for locomotion such as movement speed, direction, and turnin g angle significantly increased in the second task. Furthermore, 6 of 31 place neurons tested with the third task, in which the reward place was located outside the original place field, shifted place fields. T he results indicated that neuronal correlates of most place neurons fl exibly increased their sensitivity to relevant information in a given context and environment, and some place neurons changed the place fiel d per se with place reward association. These results suggest two stra tegies for how hippocampal neurons incorporate an incredible variety o f perceptions into a unified representation of the environment: throug h flexible use of information and the creation of new representations.