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Keywords:

  • long-term potentiation;
  • homosynaptic plasticity;
  • heterosynaptic plasticity;
  • NMDA receptors;
  • supramammillary nucleus;
  • median raphe nucleus

Abstract

The theta rhythm is the largest extracellular synchronous signal that can be recorded from the mammalian brain, and has been strongly implicated in mnemonic functions of the hippocampus. We advance the proposal that the theta rhythm represents a “tag” for short-term memory processing in the hippocampus. We propose that the hippocampus receives two main types of input, theta from ascending brainstem-diencephalo-septal systems and “information bearing” mainly from thalamocortical and cortical systems. The temporal convergence of activity of these two systems results in the encoding of information in the hippocampus, primarily reaching it via cortical routes. By analogy to processes associated with long-term potentiation (LTP), we suggest that theta represents a strong depolarizing influence on NMDA receptor-containing cells of the hippocampus. The temporal coupling of a theta-induced depolarization and the release of glutamate to these cells from intra- and extrahippocampal sources activates them. This, in turn, initiates processes leading to a (short-term) strengthening of connections between presynaptic (“information bearing”) and postsynaptic neurons of the hippocampus. Theta is selectively present in the rat during active exploratory movements. During exploration, a rat continually gathers and updates information about its environment. If this information is temporally coupled to theta (as with the case of locomotion), it becomes temporarily stored in the hippocampus by mechanisms similar to the early phase of LTP (E-LTP). If the exploratory behavior of the rat goes unreinforced, these relatively short-lasting traces (1–3 h) gradually weaken and eventually fade—to be reupdated. On the other hand, if the explorations of the rat lead to rewards (or punishments), additional modulatory inputs to the hippocampus become activated and convert the short-term, theta-dependent memory, into long-term stores. © 2005 Wiley-Liss, Inc.