Elsevier

Neural Networks

Volume 15, Issues 4–6, June–July 2002, Pages 507-521
Neural Networks

2002 Special issue
Dopamine-dependent plasticity of corticostriatal synapses

https://doi.org/10.1016/S0893-6080(02)00045-XGet rights and content

Abstract

Knowledge of the effect of dopamine on corticostriatal synaptic plasticity has advanced rapidly over the last 5 years. We consider this new knowledge in relation to three factors proposed earlier to describe the rules for synaptic plasticity in the corticostriatal pathway. These factors are a phasic increase in dopamine release, presynaptic activity and postsynaptic depolarisation. A function is proposed which relates the amount of dopamine release in the striatum to the modulation of corticostriatal synaptic efficacy. It is argued that this function, and the experimental data from which it arises, are compatible with existing models which associate the reward-related firing of dopamine neurons with changes in corticostriatal synaptic efficacy.

Introduction

Recent electrophysiological studies of the basal ganglia have provided the framework for a number of computational models of reward-related learning (Doya, 2000, Montague et al., 1996, Suri and Schultz, 1999). This evidence largely originates from the work of Schultz and colleagues who have identified a reward signal encoded in the activity of midbrain dopamine neurons (Schultz, 2000). In brief, neurons in the substantia nigra pars compacta (SNc) and the adjoining midbrain areas fire short bursts of activity after the presentation of food or liquid rewards and stimuli that predict reward (Mirenowicz and Schultz, 1994, Mirenowicz and Schultz, 1996. These dopamine neurons project predominantly to the striatum (Bjorklund & Lindvall, 1986). The effects of such short, phasic activation of the dopamine neurons on neural information processing in the striatum are a crucial component of computational models of the basal ganglia. The experimental evidence concerning these effects has advanced rapidly in recent years, and may challenge the assumptions of some existing computational models. This review focuses on experimental evidence that investigates the role of dopamine in modulating the function of striatal synapses. A set of rules for synaptic plasticity in the corticostriatal pathway is proposed, based on this evidence. Such rules may need to be incorporated into future models of reward-related learning in the basal ganglia.

Section snippets

Afferent connections of the striatum

The striatum is a major site of convergence of afferents from the cerebral cortex and the SNc. These pathways converge within the striatum and terminate close to one another on individual spiny projection neurons, the principal output neurons of the striatum (Fig. 1). The spiny projection neurons effectively form a single layer between the cortical inputs and the striatal outputs, and they are also the sites at which dopaminergic inputs are integrated with cortical inputs. This implies that the

Acute effects of dopamine

Interactions between glutamate and dopamine occur both presynaptically and postsynaptically within the striatum. These neurotransmitters act at particular receptors on the pre and postsynaptic membranes. Striatal neurons, and nerve terminals immediately afferent to them, contain both ionotropic (AMPA/kainate and N-methyl-d-aspartate, NMDA, type) and metabotropic (mGluR family) glutamate receptors, and D1-like (D1, D5 subtype) and D2-like (D2, D3 and D4 subtype) dopamine receptors. The precise

Dopamine and the three-factor rule: experimental evidence

In the last 5 years, a great deal of experimental data has amassed regarding the role of various combinations of presynaptic activity, postsynaptic activity and dopamine in synaptic modification of the corticostriatal pathway. Some of this work intentionally or unintentionally addresses the earlier hypotheses. The experiments in question have mostly been performed using the corticostriatal brain slice preparation (Arbuthnott, MacLeod, & Rutherford, 1985). Using this in vitro preparation,

Phasic activation of dopamine cells induces potentiation

In order to investigate specifically the effect of phasic release of endogenous dopamine, we have recently studied the effect of stimulating the substantia nigra dopamine neurons in an intact, anaesthetised animal. Corticostriatal synaptic efficacy was measured before and after electrically activating the dopamine cells of the substantia nigra with brief trains of pulses (Reynolds & Wickens, 2000). In agreement with most in vitro studies, we found that HFS of the contralateral cortex induced

The effect of rewarding stimulation on corticostriatal synaptic efficacy

We tested the effect of reward-related stimulation on corticostriatal synaptic efficacy using intracranial self-stimulation (ICSS) as a behavioural model of reward-related learning (Olds & Milner, 1954). In this protocol, animals learnt to press a lever repeatedly for the rewarding effect of electrical stimulation of their own substantia nigra (Beninger, Bellisle, & Milner, 1977). This provided direct experimenter control over the reward signal, enabling the same reward signal to be activated

Dopamine-plasticity function

The findings from our in vivo model and established in vitro data suggest that the level of evoked dopamine release around the time of corticostriatal activation is a critical determinant of the direction of synaptic modification in the striatum. At one extreme, near total depletion of dopamine renders corticostriatal stimulation ineffective at inducing LTD (Calabresi et al., 1992a) or LTP (Centonze et al., 1999). In vitro, the drug AMPT, which depletes striatal dopamine by a lesser degree,

Other requirements for corticostriatal LTD and LTP

Our proposal of a relationship between dopamine release and the modulation of corticostriatal synaptic efficacy is not intended to disregard the contribution of other biophysical factors that have been implicated as necessary for the induction of LTD and LTP. For LTD these include the activation of group I metabotropic glutamate receptors (mGluR1s) (Calabresi et al., 1999b, Dos Santos Villar and Walsh, 1999, Gubellini et al., 2001) and activation of the enzyme nitric oxide synthase (Calabresi

Induction of synaptic plasticity by behavioural events—a hypothesis

How might this model of corticostriatal synaptic plasticity be reconciled with the known firing patterns of dopamine neurons? In the behaving monkey, a number of observations have been made that suggest that the firing of dopamine neurons reports an error between the occurrence and the prediction of reward (Schultz, 1998). Dopamine neurons are activated phasically to fire bursts in response to unpredicted rewards during learning. Their tonic activity is uninfluenced by totally predicted rewards

Conclusions

Dopamine is now known to play a role in processes leading to corticostriatal synaptic plasticity. However, experiments over recent years have only begun to elucidate its mechanism of action in these processes. Dopamine is involved in the induction of both LTD and LTP. The mandatory requirement for associated presynaptic and postsynaptic activity is consistent with a three-factor rule of heterosynaptic plasticity. The induction of LTD requires a conjunction of presynaptic activity, postsynaptic

Acknowledgements

Supported by the Health Research Council of NZ, Lottery Health Research and the NZ Neurological Foundation.

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