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The search for the neural substrate of vertebrate action selection has focused on structures in the fore- and mid-brain, particularly on the basal ganglia. Yet, the behavioural repertoire of decerebrate and neonatal animals suggests the existence of a relatively self-contained neural substrate for action selection in the brainstem. We propose that the medial reticular formation (mRF) is this substrate's main component, reviewing evidence that the mRF's inputs, outputs, and intrinsic organisation are consistent with the requirements of an action selection system. We argue that the internal architecture of the mRF is composed of interconnected neuron clusters; our quantitative model of this anatomy suggests the mRF's intrinsic circuitry constitutes a small-world network, and may have evolved to reduce axonal wiring. We use computational models to enumerate and illustrate potential configurations of action representation within the internal circuitry of the mRF. We show that each cluster's output could represent activation of an action component; thus, co-activation of a set of these clusters would lead to the coordinated behavioural response observed in the animal. New results are presented that provide evidence for an alternative scheme: inputs to the mRF are organised to contact clusters, but recruit a pattern of reticulo-spinal neurons from across clusters to generate an action. We propose that this reconciles the anatomical structure with behavioural data showing action sequencing is degraded, rather than individual actions lost, as the mRF is progressively lesioned. Finally, we consider the potential integration of the basal ganglia and mRF substrates for selection and suggest they may collectively form a layered/hierarchical control system.
All animals must continuously sequence and coordinate behaviours appropriate to both their context and current internal state if they are to survive. It is natural to wonder what parts of the nervous system – the neural substrate – evolved to carry out this action selection process. For simpler animals, like the nematode worm Caenorhabditis elegans and the leech, a circumscribed behavioural repertoire is handled by specialist neurons that direct motor responses to specific stimuli (de Bono and Maricq, 2005; Kristan et al., 2005; Stephens et al., 2008). The sensory apparatus and motor behaviours are largely a product of these animals’ ecological niche, and hence so too is the neural network that handles the action selection process.
The mammalian brain's decision mechanism may utilise a distributed network of positive feedback loops to integrate, over time, noisy sensory evidence for and against a particular choice. Such loops would mitigate the effects of noise and have the benefit of decoupling response size from the strength of evidence, which could assist animals in acting early at the first signs of opportunity or danger. This hypothesis is explored in the context of the sensorimotor control circuitry underlying eye movements, and in relation to the hypothesis that the basal ganglia serve as a central switch acting to control the competitive accumulation of sensory evidence in positive feedback loops representing alternative actions. Results, in support of these proposals, are presented from a systems-level computational model of the primate oculomotor control. This model is able to reproduce behavioural data relating strength of sensory evidence to response time and accuracy, while also demonstrating how the basal ganglia and related oculomotor circuitry might work together to manage the initiation, control, and termination of the decision process over time.
Whether it is a cheetah deciding whether its prey is veering left or right, a rabbit deciding whether that movement in the bushes is friend or foe, or a poker player wondering if his opponent has a stronger hand, infinitesimally small variations in sensory input can give rise to vastly different behavioural outcomes: the cheetah veers left and not right, the rabbit flees or continues grazing, the card player bets a month's salary or folds. The outcome of such decisions can be critical, even a matter of life or death, which is why there will have been tremendous evolutionary pressure to develop decision-making mechanisms that can extract maximal utility from limited sensory information. In this chapter, using the oculomotor system as an exemplar, we argue that the vertebrate basal ganglia (BG) are one of the results of that evolutionary pressure and explore how these structures tame and exploit positive feedback loops (henceforth PFBLs) within the brain in order to make the most of limited information.
Subcortical substrates for behavioural integration include the fore/midbrain nuclei of the basal ganglia and the hindbrain medial reticular formation. The midbrain superior colliculus requires basal ganglia disinhibition in order to generate orienting movements. The colliculus should therefore be seen as one of many competitors vying for control of the body's effector systems with the basal ganglia acting as the key arbiter.
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