The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward.

Abstract

The basal ganglia are often conceptualised as three parallel domains that include all the constituent nuclei. The ‘ventral domain’ appears to be critical for learning flexible behaviours for exploration and foraging, as it is the recipient of converging inputs from amygdala, hippocampal formation and prefrontal cortex, putatively centres for stimulus evaluation, spatial navigation, and planning/contingency, respectively. However, compared to work on the dorsal domains, the rich potential for quantitative theories and models of the ventral domain remains largely untapped, and the purpose of this review is to provide the stimulus for this work. We systematically review the ventral domain’s structures and internal organisation, and propose a functional architecture as the basis for computational models. Using a full schematic of the structure of inputs to the ventral striatum (nucleus accumbens core and shell), we argue for the existence of many identifiable processing channels on the basis of unique combinations of afferent inputs. We then identify the potential information represented in these channels by reconciling a broad range of studies from the hippocampal, amygdala and prefrontal cortex literatures with known properties of the ventral striatum from lesion, pharmacological, and electrophysiological studies. Dopamine’s key role in learning is reviewed within the three current major computational frameworks; we also show that the shell-based basal ganglia sub-circuits are well placed to generate the phasic burst and dip responses of dopaminergic neurons. We detail dopamine’s modulation of ventral basal ganglia’s inputs by its actions on pre-synaptic terminals and post-synaptic membranes in the striatum, arguing that the complexity of these effects hint at computational roles for dopamine beyond current ideas. The ventral basal ganglia are revealed as a constellation of multiple functional systems for the learning and selection of flexible behaviours and of behavioural strategies, sharing the common operations of selection-by-disinhibition and of dopaminergic modulation.

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.