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Review
. 2017 Jan;16(1):71-85.
doi: 10.1111/gbb.12309. Epub 2016 Aug 26.

Associative and sensorimotor cortico-basal ganglia circuit roles in effects of abused drugs

C M Gremel  1 , D M Lovinger  2
Affiliations
Review

Associative and sensorimotor cortico-basal ganglia circuit roles in effects of abused drugs

C M Gremel et al. Genes Brain Behav. 2017 Jan.

Abstract

The mammalian forebrain is characterized by the presence of several parallel cortico-basal ganglia circuits that shape the learning and control of actions. Among these are the associative, limbic and sensorimotor circuits. The function of all of these circuits has now been implicated in responses to drugs of abuse, as well as drug seeking and drug taking. While the limbic circuit has been most widely examined, key roles for the other two circuits in control of goal-directed and habitual instrumental actions related to drugs of abuse have been shown. In this review we describe the three circuits and effects of acute and chronic drug exposure on circuit physiology. Our main emphasis is on drug actions in dorsal striatal components of the associative and sensorimotor circuits. We then review key findings that have implicated these circuits in drug seeking and taking behaviors, as well as drug use disorders. Finally, we consider different models describing how the three cortico-basal ganglia circuits become involved in drug-related behaviors. This topic has implications for drug use disorders and addiction, as treatments that target the balance between the different circuits may be useful for reducing excessive substance use.

Keywords: Actions; addiction; associative striatum; dopamine; drugs; goal-directed; habits; learning; plasticity; sensorimotor striatum.

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Figures

Figure 1
Figure 1
Simplified schematic diagram of the three cortico-basal-ganglia loops, including indications of glutamate, GABA, and dopamine neuron projections; A) limbic loop, B) associative loop, C) sensorimotor loop. Dorsal Medial Striatum (DMS), Dorsal Lateral Striatum (DLS), Globus Pallidus external segment (GPe), Nucleus Accumbens (NAc) Substantia Nigra pars reticulata (SNr), Substantia Nigra pars compacta (SNpc), Ventral Pallidum (VP), and Ventral Tegmental Area (VTA).
Figure 2
Figure 2
Schematic representation of reported drug-related findings in Associative (light green) and Sensorimotor (tan) loops following acute (A) or chronic (B) drug exposure. Overlap between loops is indicative of general effects with no differentiation between Associative and Sensorimotor loops. Dopamine type 1-expressing neurons (D1), dopamine type 2-expressing neurons (D2), Dorsal Striatum (DS), Globus Pallidus external segment (GPe), intermediate early gene expression (IEG), long term depression (LTD), long term potentiation (LTP), medium spiny neurons (MSNs), miniature excitatory post-synaptic currents (mEPSCs), miniature inhibitory post-synaptic currents (mIPSCs), SNr (Substantia pars reticulata).
Figure 3
Figure 3
Example simplified schematic of differing models showing brain areas involved in the transition from initial drug use to addiction. A. Model where parallel striatal-midbrain loops link limbic and sensorimotor circuits, leading to gradual habitual control of actions involving Pavlovian-Instrumental transfer. B) Model where parallel associative and sensorimotor circuits mediate competing goal-directed and habitual instrumental actions, with multiple sites of circuit modulation & interaction (e.g. corticostriatal efficacy, midbrain, and basal ganglia/thalamic loops).
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