A computational perspective on the striatum

Abstract

Brain Dynamics and the Striatal Complexedited by R. Miller and J.R. Wickens. Harwood Academic Publishers, 2000. £50.00 (324 pages) 90 5702 478 0Brain Dynamics and the Striatal Complex is the first volume in a new series from Harwood Academic on Conceptual Advances in Brain Research. The series seeks to go beyond experimental and empirical advances to provide analyses of brain organization and function at more conceptual, computational and theoretical levels. Volume 1 succeeds impressively.In opening the pages, I anticipated yet another proceedings type of book, comprising independent reviews of the latest progress. By contrast, I have been captivated by a coherent series of chapters, each addressing different perspectives on the core problem of how best to integrate behavioural, pharmacological, physiological, anatomical and molecular data to understand properly the underlying function of the mammalian striatum. It is not just that the individual chapters have been commissioned to discuss different perspectives on the same issue; rather, there is a commonality of purpose by the authors, combined with extensive cross-referencing of topics and ideas between chapters, and an extended and carefully edited discussion of core themes. Finally there is an afterword by one of the contributors, Charlie Wilson, that wonderfully clarifies a core aspect of the underlying systems debate that has led to much disagreement among the participants.At the heart of the book is the question of how to integrate behavioural, physiological and structural perspectives on striatal function. The basic cell types, characterized morphologically and neurochemically, and their input and output connections, have been well established for some decades, although new refinements (reviewed by Bennett and Wilson) are constantly being updated. A bewildering variety of models of striatal circuit organization have been proposed, including topographic inputs from the whole cortical mantle, striosomes and matrix compartments internally, separate direct and indirect output projections, and organization in parallel open and closed feedback corticostriatal–thalamocortical loops. Each appears to convey important aspects of organization but when pieced together they appear confusingly incompatible. At the behavioural level, the striatum has long been associated with both motor and cognitive functions, and more recently a role has been suggested in motor and associative learning in addition to the initiation, selection and execution of motor actions (Beninger and Olmstead, Joel and Weiner), although exactly how this relates to the different principles of anatomical organization remains elusive.Electrophysiological recording of neuronal activity from behaving cats, rats and monkeys has provided considerable information on the identification of striatal projection neurones responding to convergence of cortical activation and of dopamine cell-firing with signals of reward (Hyland). This has provided the starting point for determining the principles of physiological plasticity of striatal neurones necessary to represent associative learning (Wickens). At the same time, several traditional assumptions about striatal organization are now being challenged with data from more reductionist approaches. Thus, the classical excitatory–inhibitory distinction between activation at receptors of the D1 and D2 classes is found not to be consistently supported in the single cell when studied at the molecular level (Surmeier), and long-standing assumptions about convergence between domains or modules of medium spiny striatal neurones and their pallidal targets being mediated by recurrent lateral inhibition (e.g. Oorschot, Joel and Weiner) is found to be difficult to reconcile with actual physiological data or with quantitative models of the local circuits (Plenz and Kitai, Wilson). These considerations are now leading to refined conceptual and theoretical models of the nature of information processing by striatal neurones embedded within wider brain circuits, and suggest for the first time valid deterministic models of striatal function.Brain Dynamics and the Striatal Complex conjures up the excitement of contemporary striatal research. It is written with a lucidity that is accessible to the non-specialist but still maintains the intellectual rigour of the expert theoretician. Inevitably, in a slim volume, several key players in the debate are not represented as authors (Arbuthnott, Graybiel and Robbins among them) but their work is not neglected in the reviews and discussions present. There remains here a book of exceptional interest lying hidden behind its modest covers.