2002 Special issue Dopamine-dependent plasticity of corticostriatal synapses John N.J. Reynolds, Jeffery R. Wickens * The Neuroscience Research Centre and Department of Anatomy and Structural Biology, School of Medical Sciences, University of Otago, P.O. Box 913, Dunedin, New Zealand Received 6 November 2001; revised 25 February 2002; accepted 25 February 2002 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. q 2002 Elsevier Science Ltd. All rights reserved. Keywords: Dopamine; Striatum; Corticostriatal; Reward; Learning; Plasticity 1. 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, Dayan, & Sejnowski, 1996; Suri & 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 & Schultz, 1994, 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. 2. 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 functional properties of the corticostriatal synapses, the response properties of spiny projection neurons and the effects of dopamine on these properties are key determinants of the signal processing operations in the striatum. The corticostriatal projection originates from all areas of the cerebral cortex (McGeorge & Faull, 1989) and releases glutamate into the striatum (Divac, Fonnum, & Storm-Mathisen, 1977; Perschak & Cuenod, 1990). The axon terminals form asymmetric specialisations with the heads of dendritic spines of spiny projection neurons (Somogyi, Bolam, & Smith, 1981). Dopaminergic axons of the nigrostriatal pathway synapse with the dendrites and somata of spiny projection neurons, and also with dendritic 0893-6080/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S0893-6080(02)00045-X Neural Networks 15 (2002) 507–521 www.elsevier.com/locate/neunet * Corresponding author. Tel.: þ 64-3-479-7373; fax: þ64-3-479-7254. E-mail address: jeff.wickens@stonebow.otago.ac.nz (J.R. Wickens).