The Journal of Neurophysiology Vol. 78 No. 2 August 1997, pp. 597-613
Copyright ©1997 The American Physiological Society

Task-Dependent Representations in Rat Hippocampal Place Neurons

Tsuneyuki Kobayashi¹, Hisao Nishijo¹, Masaji Fukuda¹, Jan Bures², and Taketoshi Ono¹

¹ Department of Physiology, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Toyama 930-01, Japan; and ² Institute of Physiology, Academy of Sciences, 142 20 Prague 4-Krc, Czech Republic

Kobayashi, Tsuneyuki, Hisao Nishijo, Masaji Fukuda, Jan Bures, and Taketoshi Ono. Task-dependent representations in rat hippocampal place neurons. J. Neurophysiol. 78: 597-613, 1997. It is suggested that the hippocampal formation is essential to spatial representations by flexible encoding of diverse information during navigation, which includes not only externally generated sensory information such as visual and auditory sensation but also ideothetic information concerning locomotion (i.e., internally generated information such as proprioceptive and vestibular sensation) as well as information concerning reward. In the present study, we investigated how various types of information are represented in the hippocampal formation, by recording hippocampal complex-spike cells from rats that performed three types of place learning tasks in a circular open field with the use of intracranial self-stimulation as reward. The intracranial self-stimulation reward was delivered in the following three contexts: if the rat 1) entered an experimenter-determined reward place within the open field, and this place was randomly varied in sequential trials; 2) entered two specific places, one within and one outside the place field (an area identified by change in activity of a place neuron); or 3) entered an experimenter-specified place outside the place field. Because the behavioral trails during navigation were more constant in the second task than in the first task, ideothetic information concerning locomotion was more relevant to acquiring reward in the second task than in the first task. Of 43 complex-spike cells recorded, 37 displayed place fields under the first task. Of these 37 place neurons, 34 also had significant reward correlates only inside the place field. Although reward 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 turning 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. The results indicated that neuronal correlates of most place neurons flexibly increased their sensitivity to relevant information in a given context and environment, and some place neurons changed the place field per se with place reward association. These results suggest two strategies for how hippocampal neurons incorporate an incredible variety of perceptions into a unified representation of the environment: through flexible use of information and the creation of new representations.

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