Elsevier

Brain Research

Volume 1628, Part A, 2 December 2015, Pages 104-116
Brain Research

Research Report
Thalamocortical integration of instrumental learning and performance and their disintegration in addiction

https://doi.org/10.1016/j.brainres.2014.12.023Get rights and content

Highlights

  • Drug addiction causes deficits in cognitive and emotional processes.

  • We contend that drug exposure also affects cognitive–emotional integration.

  • We hypothesize that this integration emerges in the thalamocortical network.

Abstract

A recent focus of addiction research has been on the effect of drug exposure on the neural processes that mediate the acquisition and performance of goal-directed instrumental actions. Deficits in goal-directed control and a consequent dysregulation of habit learning processes have been described as resulting in compulsive drug seeking. Similarly, considerable research has focussed on the motivational and emotional changes that drugs produce and that result in changes in the incentive processes that modulate goal-directed performance. Although these areas have developed independently, we argue that the effects they described are likely not independent. Here we hypothesize that these changes result from a core deficit in the way the learning and performance factors that support goal-directed action are integrated at a neural level to maintain behavioural control. A dorsal basal ganglia stream mediating goal-directed learning and a ventral stream mediating various performance factors find several points of integration in the cortical basal ganglia system, most notably in the thalamocortical network linking basal ganglia output to a variety of cortical control centres. Recent research in humans and other animals is reviewed suggesting that learning and performance factors are integrated in a network centred on the mediodorsal thalamus and that disintegration in this network may provide the basis for a ‘switch’ from recreational to dysregulated drug seeking resulting in the well documented changes associated with addiction.

This article is part of a Special Issue entitled SI:Addiction circuits.

Section snippets

Instrumental learning

It has long been recognised that what an animal does is of little use in establishing what that animal has learned; that, whether an animal responds similarly or very differently across conditions, common or quite distinct learning processes could be at play across those conditions (Tolman, 1952, Tolman, 1948). One of the clearest examples of this observation comes from studies of instrumental conditioning in which animals are trained to perform relatively arbitrary actions in order to gain

Instrumental performance

Over and above these learning processes, instrumental conditioning is strongly influenced by a range of performance factors from basic regulatory processes, including motivational manipulations that exert a general arousal or activating effect, to those exerting more selective control, affecting the vigor of, or choice between, specific actions. With regard to these latter specific influences on performance, there are two primary categories: factors that influence the reward value of the

The integration of learning and motivation in the dorsal and ventral streams

In line with the above analysis and by analogy to the functional anatomy of the visual system, we recently suggested that the dorsal and ventral striatal networks through the basal ganglia be considered as two ‘streams’, mediating distinct learning and performance functions in instrumental conditioning (Hart et al., 2014). This suggestion implies that the integration of learning and performance should take place in the integration of these streams. Furthermore, given the motivational and

Implications for studying addiction

These data are, at present, long on promise but, together with the rodent data, they provide some impetus to the hypothesis that deficits in goal-directed action control not only emerge from damage to the circuitry involved in specific learning and performance processes but also to circuits within the MDT and the thalamocortical circuit more generally that we hypothesize mediate the interaction between them. From the perspective of addiction, these ideas point to a potential target for research

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  • Cited by (0)

    The preparation of this manuscript was supported by a Laureate Fellowship from the Australian Research Council #FL0992409 to BWB and National Alliance for Research on Schizophrenia and Depression Young Investigator Award from the Brain & Behavior Research Foundation to RWM.

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