AbstractÑA selection problem arises whenever two or more competing systems seek simultaneous access to a restricted resource. Consideration of several selection architectures suggests there are significant advantages for systems which incorporate a central switching mechanism. We propose that the vertebrate basal ganglia have evolved as a centralised selection device, specialised to resolve conflicts over access to limited motor and cognitive resources. Analysis of basal ganglia functional architecture and its position within a wider anatomical framework suggests it can satisfy many of the requirements expected of an efficient selection mechanism.
Progressive loss of the ascending dopaminergic projection in the basal ganglia is a fundamental pathological feature of Parkinson's disease. Studies in animals and humans have identified spatially segregated functional territories in the basal ganglia for the control of goal-directed and habitual actions. In patients with Parkinson's disease the loss of dopamine is predominantly in the posterior putamen, a region of the basal ganglia associated with the control of habitual behaviour. These patients may therefore be forced into a progressive reliance on the goal-directed mode of action control that is mediated by comparatively preserved processing in the rostromedial striatum. Thus, many of their behavioural difficulties may reflect a loss of normal automatic control owing to distorting output signals from habitual control circuits, which impede the expression of goaldirected action.The basal ganglia are a group of subcortical nuclei that have been linked to movement control since the end of the nineteenth century when David Ferrier concluded that the corpus striatum contained "the centres of automatic or sub-voluntary integration" (REF. 1 Europe PMC Funders Author ManuscriptsEurope PMC Funders Author Manuscripts view was expanded in the early twentieth century by observations that basal ganglia lesions were associated with movement disorders (BOX 1). The first functional model of basal ganglia architecture was developed in the late 1980s (FIG. 1a). In this model, cortical inputs enter the basal ganglia through the striatum (in primates this consists of the caudate nucleus and the putamen), and the internal globus pallidus (GPi) and the substantia nigra pars reticulata (SNr) serve as the principal output nuclei. The activity of striatal medium spiny projection neurons is conveyed to the output nuclei (GPi and SNr) through a monosynaptic GABA (γ-aminobutyric acid)-ergic projection (the 'direct' pathway) and a polysynaptic ('indirect') pathway that involves relays in the external globus pallidus (GPe) and the subthalamic nucleus (STN) 2 , 3 . Output from GABAergic GPi and SNr neurons keep targeted structures in the thalamus and brainstem under tonic inhibitory control: this tonic inhibition is blocked (that is, paused) by phasic inhibitory signals from the 'direct' striato-nigralpallidal projection 4 , which releases thalamocortical and brainstem structures from inhibition, thereby allowing movement to proceed. Dopaminergic input from the substantia nigra pars compacta (SNc) modulates corticostriatal transmission by exerting a dual effect on striatal projection neurons (FIG. 1). Neurons that co-express dopamine D1 receptors, substance P and dynorphin and give rise to the 'direct pathway' are excited by dopamine, whereas neurons that co-express D2 receptors and encephalin, and that give rise to the 'indirect pathway', are inhibited 5 (FIG. 1a). Consequently, according to this model, in the normal state, activation of the 'indirect circuits' at the level of the striatum would promote movement inhibition or...
An influential concept in contemporary computational neuroscience is the reward prediction error hypothesis of phasic dopaminergic function. It maintains that midbrain dopaminergic neurons signal the occurrence of unpredicted reward, which is used in appetitive learning to reinforce existing actions that most often lead to reward. However, the availability of limited afferent sensory processing and the precise timing of dopaminergic signals suggest that they might instead have a central role in identifying which aspects of context and behavioural output are crucial in causing unpredicted events.
We present a biologically plausible model of processing intrinsic to the basal ganglia based on the computational premise that action selection is a primary role of these central brain structures. By encoding the propensity for selecting a given action in a scalar value (the salience), it is shown that action selection may be recast in terms of signal selection. The generic properties of signal selection are defined and neural networks for this type of computation examined. A comparison between these networks and basal ganglia anatomy leads to a novel functional decomposition of the basal ganglia architecture into 'selection' and 'control' pathways. The former pathway performs the selection per se via a feedforward off-centre on-surround network. The control pathway regulates the action of the selection pathway to ensure its effective operation, and synergistically complements its dopaminergic modulation. The model contrasts with the prevailing functional segregation of basal ganglia into 'direct' and 'indirect' pathways.
Unexpected stimuli which are behaviourally significant have the capacity to evoke a short latency, short duration burst of firing in mesencephalic dopamine neurones. An influential interpretation of the experimental data characterising this response proposes that dopamine neurones play a critical role in reinforcement learning by signalling errors in the prediction of future reward. In the present viewpoint we propose a different functional role for the short latency dopamine response in the mechanisms of associative learning.We suggest that the initial burst of dopaminergic firing may represent an essential component in the process of switching attentional and behavioural selections to unexpected, behaviourally important stimuli. This switching response could be a critical prerequisite for associative learning and may be part of a general short latency reaction, mediated by catecholamines, which prepares the organism to react appropriately to biologically significant events. Introduction:ÒAny act which in a given situation produces satisfaction becomes associated with that situation so that when the situation recurs the act is more likely than before to recur alsoÓ. Although the effects of positive and negative reinforcement on behaviour have been known for centuries, Thorndike 1 in this statement formalised the linking of action to situation on the basis of outcome. It also emphasises two of the principal functions of rewarding or appetitive stimuli: to produce satisfaction (hedonia) and to adjust the probabilities of selecting immediately preceding actions. A third, often recognised function of rewarding stimuli is to elicit approach and consummatory behaviour 2 . While the neural mechanisms mediating any of these processes have yet to be identified in detail, much evidence points to the vertebrate basal ganglia playing a central role 3 . Numerous investigations of this system using a wide range of experimental techniques suggest that ascending dopaminergic projections from the ventral midbrain (substantia nigra pars compacta (SNc) and the ventral tegmental area (VTA)) to the striatum (caudate, putamen and nucleus accumbens) provide essential signals for reinforcement learning 2, 4, 5 . Currently, a popular view is that dopaminergic input to the striatum provides the reinforcement signal required to adjust the probabilities of subsequent action selection [4][5][6][7] . A particularly important and influential part of the evidence supporting this view concerns the short latency, short duration response of dopamine cells observed after the unexpected presentation of a behaviourally significant stimulus 2,8 . This response has been widely interpreted as providing the system with a reinforcement prediction error signal 5, 9 . We will, however, argue that the short latency burst of dopamine activity could have a rather different functional role. Specifically, we suggest that the short latency response may represent an important component of the processes responsible for re-allocating attentional and behavioural re...
In a companion paper a new functional architecture was proposed for the basal ganglia based on the premise that these brain structures play a central role in behavioural action selection. The current paper quantitatively describes the properties of the model using analysis and simulation. The decomposition of the basal ganglia into selection and control pathways is supported in several ways. First, several elegant features are exposed--capacity scaling, enhanced selectivity and synergistic dopamine modulation--which might be expected to exist in a well designed action selection mechanism. The discovery of these features also lends support to the computational premise of selection that underpins our model. Second, good matches between model globus pallidus external segment output and globus pallidus internal segment and substantia nigra reticulata area output, and neurophysiological data, have been found which are indicative of common architectural features in the model and biological basal ganglia. Third, the behaviour of the model as a signal selection mechanism has parallels with some kinds of action selection observed in animals under various levels of dopaminergic modulation.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.