The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward.
Introduction
The basal ganglia, a group of inter-connected nuclei in the vertebrate fore- and mid-brain, form the centre of a vast literature. This literature can be roughly divided by its focus on either the dorsal or ventral parts of the basal ganglia, and corresponding research themes of workers in those two fields. Computational models, whether explicitly stated or not, focus almost exclusively on the dorsal basal ganglia (e.g. Contreras-Vidal and Stelmach, 1995, Beiser and Houk, 1998, Berns and Sejnowski, 1998, Gurney et al., 2001b, Humphries et al., 2006, Leblois et al., 2006), in large part because of the large number of available systematic reviews of the dorsal basal ganglia (e.g. Parent and Hazrati, 1995, Gerfen and Wilson, 1996, Mink, 1996, Redgrave et al., 1999a, Bolam et al., 2000, Gurney et al., 2001a). We present this review and synthesis to provide the same level of systematically organised information, sufficient for building computational models that are specific to ventral basal ganglia, and to stimulate further development of quantitative, theoretical thinking in this field. Our aim is to also to help bridge the surprisingly disparate literatures on the dorsal and ventral basal ganglia. We build here on previous excellent reviews of the ventral basal ganglia, particularly (Pennartz et al., 1994, Groenewegen et al., 1999b, Groenewegen et al., 1999c, Ikemoto, 2007, Nicola, 2007). Our functional focus in particular is on the key role they appear to play in exploration and foraging (Swanson, 2000, Zahm, 2006) through the co-ordination of spatial navigation, reward evaluation, and behavioural strategy.
A note on neuroscience terminology is appropriate at this point to orient the computationally inclined reader. The names and boundaries given to brain structures are often the focus of fierce debate. Divisions made on anatomical grounds of, for example, neuron shape and size may not correlate with divisions that could be made based on neurotransmitter content, or projection targets, or sources of afferent inputs. Ideally, a definable brain structure has unique combinations of all these properties; yet these are all structural properties, and may ultimately not correlate with the functional properties of those neurons, such as their response to the sound or colour of a stimulus. Thus, here, as is often the case in discussions of the brain, it is not possible to cleanly separate the structural and functional aspects, as each informs and constrains the other. In what follows, we use data and brain terminology mostly derived from rat studies. This approach is adopted to ensure consistency and compatibility when interpreting results from different studies, because the rat brain is the best studied of all vertebrates. Corroborating evidence from other species is discussed where available.
Section snippets
A basal ganglia primer
We begin by outlining the classic model of anatomy that is often simply labelled ‘basal ganglia’, despite, as will become clear, only strictly applying to the dorsal basal ganglia. This will provide a useful point of comparison for the elaboration of the ventral basal ganglia. Such treatments of classic basal ganglia anatomy identify six main structures (Bolam et al., 2000), illustrated in Fig. 1a. The striatum forms the largest part of the basal ganglia, and is the primary input nucleus. The
A new functional anatomy of the ventral basal ganglia
Our model for the functional anatomy of the ventral basal ganglia is shown in Fig. 2. A “functional anatomy” attempts to describe the connections and nuclei divisions that are key to the putative function of the brain region (more on this below). It leaves aside minor connections between structures, as defined by small numbers of terminals, very minor neuron populations, as defined by percentage composition of a nucleus, and, at this level of analysis, some internal structure of the nuclei,
Dopamine and the striatum
We review here the types, distribution, and activation effects of dopamine receptors, in part to flesh out some of the above assertions about dopamine receptor expression, in part to provide some understanding of why dopamine has a central place in the ventral striatum research, and in part to underscore the difficulty of relating dopamine to behaviour. We draw from literature across the whole striatum, as the dorsal and ventral striatum have much in common, and there is a far larger body of
Information carried by the primary inputs to the ventral basal ganglia
The ventral striatum has a common input structure with the dorsal striatum, as both receive input from neocortex, thalamus, and the dopaminergic neuron bands of the brainstem. Neocortical input originates mostly from prefrontal cortex, which extends its projections across the dorsomedial striatum too. What makes ventral striatum unique is its inputs from the hippocampal formation and basal amygdala complex (though the latter extends a little into dorsomedial striatum). If we are to understand
Behavioural roles of the ventral striatum
How then are all these inputs combined to shape behaviour? We briefly review here insight from behavioural assays following lesion, inactivation or chemical manipulation of NAcc sub-regions, and from NAcc neural activity correlates of behaviour.
Convergence of inputs: channels within the basal ganglia
What substrate underpins the computations of the basal ganglia, using the combinations of the afferent information, and giving rise to the correlates of ventral striatal activity? A central concept governing the organisation of basal ganglia connectivity is the existence of parallel anatomical loops — channels — running throughout the basal ganglia nuclei (Alexander et al., 1986, Middleton and Strick, 2000). A distinction can be made between macroscopic and microscopic channels.
A roadmap for quantitative models of ventral basal ganglia
We bring together the above work on the functional architecture, input distribution, functions of afferent domains, and correlates of NAcc manipulations and activity into a roadmap for developing a more complete understanding of the ventral basal ganglia.
Conclusions
The ventral basal ganglia domain can be cleanly divided in two. On one hand, the nucleus accumbens core and associated regions of other basal ganglia nuclei form a clear homologue of the dorsolateral and dorsomedial basal ganglia, and so we extend the selection hypothesis to this circuit too. On the other, the nucleus accumbens shell sits as the gateway to a much simplified basal ganglia circuit, but also to more complex interactions directly with the rest of the brain. Within these divisions,
Acknowledgements
We thank Peter Redgrave for comments on earlier versions of this manuscript; and Mehdi Khamassi for stimulating feedback, new literature sources, and drawing our attention to some of the problems in the ventral striatal literature. This work was funded by the European Union Framework 6 IST 027819 ICEA project.
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