Dopamine: a potential substrate for synaptic plasticity and memory mechanisms
Introduction
The idea that an additional mechanism was necessary for the N-methyl-d-aspartate (NMDA) receptor-dependent long-term potentiation (LTP) to produce a long-lasting maintenance of several hours was suggested by the fact that neither N-methyl-d-aspartate alone or in combination with other glutamatergic agonists was able to produce a non-decremental LTP (Kauer et al., 1988). The involvement of aminergic influences on LTP was first considered when two studies concurrently demonstrated that a depletion of 5-hydroxytryptamine (5 HT) or global catecholamine could modulate LTP in the dentate gyrus of freely moving rats (Bliss et al., 1983, Krug et al., 1983). In the field of catecholamine transmitters, dopamine (DA) pathways have then been recognized to play a critical role in cognition and emotion, and the last decade has seen a large increase in the experimental evidence for a role of DA in both synaptic plasticity and memory processes. The cloning of five DA receptors and the development of more specific agonists and antagonists of the different DA receptors have helped in characterizing the action of DA on synaptic plasticity. Concomitantly, sophisticated behavioral paradigms have let us progress in elucidating the role of DA in cognition.
A large number of different paradigms have been used to examine the role of DA in synaptic plasticity in mostly three brain regions innervated by DA: the striatum including the nucleus accumbens, the hippocampus and the prefrontal cortex. Studies in the striatum have been reviewed by Lovinger and Tyler (1996), Arbuthnott et al. (2000) and Centonze et al. (2001a) and data in the hippocampus summarized by Lisman and Otmakhova (2001) in an extension of their network model of hippocampal function. The focus of this review is on the coverage of data collected over the last decade on DA and synaptic plasticity in the striatum, nucleus accumbens, hippocampus and prefrontal cortex. The first part of the review provides an overview of the modulatory effects of DA on synaptic plasticity including LTP, long-term depression (LTD) and depotentiation in these different brain regions innervated by midbrain DA systems. For each region considered, a short summary on DA innervation and DA receptor distribution has been included or appropriate review articles referenced. The description of a possible cellular mechanism of action of DA on LTP is then outlined. The second part of the review addresses the functions of hippocampal, striatal or prefrontal DA systems in different forms of memories as assessed with behavioral, pharmacological or lesion studies, and a few experiments on cellular mechanisms underlying the function of DA in memory processes are summarized. The conclusion is an attempt to compare the function of DA in the memory processes with its role in synaptic plasticity.
Section snippets
Dopamine and synaptic plasticity
Since the discovery of LTP in the hippocampus (Bliss and Lomo, 1973), synapses that undergo plastic changes have been described in various parts of the brain and particularly in brain regions that receive DA innervations. It is now well established that the strength of synaptic transmission can be modified on a long-term basis by specific patterns of activation such as high frequency trains that produce LTP, and also by the action of endogenous modulators such as DA. Using different in vitro or
Interaction of dopaminergic systems with memory processes
Different approaches from unit recording to lesion and pharmacological studies have demonstrated that DA plays a critical role in the modulation of neuronal activities that are related to different forms of learning and memory. It is beyond the scope of this review to summarize the effects of DA on all types of memory. Rather, major studies dealing with local prefrontal, hippocampal or striatal DA systems and different forms of memories will be summarized and compared to DA modulation of
Interaction of dopamine and glutamate systems on local circuits
The existing data show an heterogeneous action of DA in the different structures examined and controversies still remain on this topic. However, DA receptor activation appears to be important in expressing either LTP and/or LTD in all regions examined. To understand the cellular basis of the interactions of DA and glutamate systems during these different forms of plasticity, it will be important to learn which specific cells and which specific receptors are the targets of DA terminals and how
Conclusion
Synaptic plasticity induced in the different regions examined (hippocampus, striatum and prefrontal cortex) does not appear to recruit the DA systems in similar manners. It is conceivable that a local regulation of these plastic events is specific to the region where the synapses are activated. Although a comparable DA modulation appears to be present in the hippocampus and the prefrontal cortex, only the consolidation of LTP in the hippocampus is dependent on D1 receptors whereas a potential
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