Dopamine: a potential substrate for synaptic plasticity and memory mechanisms

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Abstract

It is only recently that a number of studies on synaptic plasticity in the hippocampus and other brain areas have considered that a heterosynaptic modulatory input could be recruited as well as the coincident firing of pre- and post-synaptic neurons. So far, the strongest evidence for such a regulation has been attributed to dopaminergic (DA) systems but other modulatory pathways have also been considered to influence synaptic plasticity. This review will focus on dopamine contribution to synaptic plasticity in different brain areas (hippocampus, striatum and prefrontal cortex) with, for each region, a few lines on the distribution of DA projections and receptors. New insights into the possible mechanisms underlying these plastic changes will be considered. The contribution of various DA systems in certain forms of learning and memory will be reviewed with recent advances supporting the hypothesis of similar cellular mechanisms underlying DA regulation of synaptic plasticity and memory processes in which the cyclic adenosine monophosphate/protein kinase A (cAMP/PKA) pathway has a potential role. To summarize, endogenous DA, which depends on the activity patterns of DA midbrain neurons in freely moving animals, appears as a key regulator in specific synaptic changes observed at certain stages of learning and memory and of synaptic plasticity.

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

References (159)

  • M.C. Defagot et al.

    Distribution of D4 dopamine receptor in rat brain with sequence-specific antibodies

    Brain Res. Mol. Brain Res.

    (1997)
  • F. Dos Santos Villar et al.

    Modulation of long-term synaptic plasticity at excitatory striatal synapses

    Neuroscience

    (1999)
  • T.F. Freund et al.

    Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines

    Neuroscience

    (1984)
  • U. Frey et al.

    Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices

    Brain Res.

    (1990)
  • U. Frey et al.

    The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro

    Neurosci. Lett.

    (1991)
  • A. Gasbarri et al.

    Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat

    Brain Res. Bull.

    (1994)
  • A. Gasbarri et al.

    Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat

    Neuroscience

    (1996)
  • P.S. Goldman-Rakic et al.

    D(1) receptors in prefrontal cells and circuits

    Brain Res. Brain Res. Rev.

    (2000)
  • V.K. Gribkoff et al.

    Modulation by dopamine of population responses and cell membrane properties of hippocampal CA1 neurons in vitro

    Brain Res.

    (1984)
  • H. Gurden et al.

    Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation

    Neuroscience

    (1999)
  • H. Hortnagl et al.

    Regional heterogeneity in the distribution of neurotransmitter markers in the rat hippocampus

    Neuroscience

    (1991)
  • A. Jansson et al.

    On the distribution patterns of D1, D2, tyrosine hydroxylase and dopamine transporter immunoreactivities in the ventral striatum of the rat

    Neuroscience

    (1999)
  • T.M. Jay et al.

    Plasticity of the hippocampal-prefrontal cortex synapses

    J. Physiol. Paris

    (1996)
  • Z.U. Khan et al.

    Dopamine D5 receptors of rat and human brain

    Neuroscience

    (2000)
  • M. Krug et al.

    Aminergic blockade modulates long-term potentiation in the dentate gyrus of freely moving rats

    Brain Res. Bull.

    (1983)
  • S. Laroche et al.

    Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region

    Neurosci. Lett.

    (1990)
  • D. Law-Tho et al.

    Dopamine favours the emergence of long-term depression versus long-term potentiation in slices of rat prefrontal cortex

    Neurosci. Lett.

    (1995)
  • J.E. Lisman et al.

    A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly

    Neuron

    (2001)
  • F.C. Liu et al.

    Spatiotemporal dynamics of CREB phosphorylation: transient versus sustained phosphorylation in the developing striatum

    Neuron

    (1996)
  • D.M. Lovinger et al.

    Synaptic transmission and modulation in the neostriatum

    Int. Rev. Neurobiol.

    (1996)
  • R.C. Malenka et al.

    Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells

    Brain Res.

    (1986)
  • E. Miyoshi et al.

    Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions

    Brain Res. Bull.

    (2002)
  • R.D. Oades et al.

    Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity

    Brain Res.

    (1987)
  • T. Aosaki et al.

    Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning

    J. Neurosci.

    (1994)
  • G.W. Arbuthnott et al.

    Dopamine and synaptic plasticity in the neostriatum

    J. Anat.

    (2000)
  • H. Aujla et al.

    Hippocampal-prefrontocortical circuits: PKA inhibition in the prefrontal cortex impairs delayed nonmatching in the radial maze in rats

    Behav. Neurosci.

    (2001)
  • A.E. Baldwin et al.

    Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex

    J. Neurosci.

    (2002)
  • L.S. Benardo et al.

    Dopamine action on hippocampal pyramidal cells

    J. Neurosci.

    (1982)
  • C. Bergson et al.

    Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain

    J. Neurosci.

    (1995)
  • R. Bernabeu et al.

    Further evidence for the involvement of a hippocampal cGMP/cGMP-dependent protein kinase cascade in memory consolidation

    NeuroReport

    (1997)
  • T.V. Bliss et al.

    Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path

    J. Physiol.

    (1973)
  • T.V. Bliss et al.

    Reduction of long-term potentiation in the dentate gyrus of the rat following selective depletion of monoamines

    J. Physiol.

    (1983)
  • R.D. Blitzer et al.

    Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP

    Science

    (1998)
  • R. Bourtchouladze et al.

    Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA

    Learn. Mem.

    (1998)
  • T.J. Brozoski et al.

    Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey

    Science

    (1979)
  • P. Calabresi et al.

    Long-term synaptic depression in the striatum: physiological and pharmacological characterization

    J. Neurosci.

    (1992)
  • P. Calabresi et al.

    Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels

    Eur. J. Neurosci.

    (1992)
  • P. Calabresi et al.

    Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson’s disease

    Brain

    (1993)
  • P. Calabresi et al.

    Transmitter release associated with long-term synaptic depression in rat corticostriatal slices

    Eur. J. Neurosci.

    (1995)
  • P. Calabresi et al.

    Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors

    J. Neurosci.

    (1997)
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