How the Basal Ganglia Make Decisions

Abstract

The primate basal ganglia are a collection of subcortical structures that have long been considered part of the extrapyramidal motor system, the part of the motor system concerned with automatic aspects of movement. Despite a large amount of data regarding their anatomy and physiology, the role of the basal ganglia in both action planning and decision making remains enigmatic. Anatomical labeling studies have suggested that the striatum receives projections from the cerebral cortex that coarsely preserves topography, and that the basal ganglia maintain a segregation of information streams (Goldman-Rakic and Selemon 1986;Hoover and Strick 1993;Parent 1990). We suggest that the connectivity of the basal ganglia is ideally suited to selecting optimal actions for given cognitive and sensory states. We demonstrate how a computational network of pools of neurons connected in the arrangement found in the basal ganglia can perform what we term a "winnerlose-all" function. The winner-lose-all mechanism refers to the fact that the neurons of the output stage of the basal ganglia, the internal segment of the globus pallidus (GPi), are tonically active and are inhibited when corresponding striatal afferents fire. Thus the GPi neuron that is selected is actually inhibited because it loses rather than wins the competition. Diffuse excitatory projections from the subthalamic nucleus prevent all but the winning pallidal neuron pool from being inhibited. Because the thalamic targets of the GPi projection in turn feed back to the approximate cortical area of the originating afferent, this cortical-subcortical loop is ideally suited not only for the aforementioned action-selection, but also for the generation of sequences appropriate for given cortical states. We demonstrate how the circuitry of the basal ganglia can learn to select the best action for different cortical states and how the feedback representation of the action-selection leads to the generation of sequences of actions.

Response selection involves executive control: Evidence from the selective interference paradigm

“…The observation that the simple RT task was more adversely affected in a dual-task setting than the choice RT task was replicates earlier findings of Frith and Done (1986), who also observed a greater dual-task cost in RT performance for a simple (24%) than for a choice (8%) RT task. Such results are taken to indicate that simple and choice RT tasks follow different neural routes and, thus, are considered to be qualitatively different (see also Berns & Sejnowski, 1996;Rowe et al, 2000;Schubert, 1999). A final remark is related to the longer processing time observed in choice reaction than in simple reaction.…”

Modeling functions of striatal dopamine modulation in learning and planning

“…Since there is strong convergence from cortex via striatal matrisomes to the basal ganglia output nuclei (Alexander et al, 1986), only the predominant striatal activity may be represented in the firing rates of the output nuclei. We implement a selection mechanism according to the proposal of Berns and Sejnowski (1996), who demonstrated in simulation experiments that this selection may be caused by the projections of the indirect pathway via the globus pallidus exterior (GPe) and the subthalamic nucleus (STN). Their results suggest that the indirect pathway selects the predominant representations by disinhibiting minor suppressions of neural activities in the basal ganglia output nuclei.…”

“…For simplicity, we call these neuron populations "(simulated) neurons". Following the proposal of Berns and Sejnowski (1996), we assume that only the predominant striatal firing rate is represented in the basal ganglia output nuclei globus pallidus interior (GPi) and substantia nigra pars reticulata (SNr) and projected via thalamus to cortical areas. Strong and persistent depressions of firing rates in these basal ganglia output nuclei elicit acts via thalamocortical projections.…”

“…The firing rates y 1 (t) and y 2 (t) of both striatal neurons inhibit the basal ganglia output nuclei substantia nigra pars reticulata (SNr) and globus pallidus interior (GPi). An indirect disinhibitory pathway from striatum to GPi/SNr suppresses insignificant inhibitions in the basal ganglia output nuclei (Berns and Sejnowski, 1996). The winning inhibition disinhibits the thalamus.…”

The Integrative Role of the Basal Ganglia

“…However, the exact aspects of motor control that they have under normal conditions have not been clear at all. The traditional view is that the basal ganglia are involved in the selection and inhibition of action commands [2], but an increasing number of brain-imaging studies show that the basal ganglia, besides being involved in motor tasks are also involved in more integrative and cognitive processes such as mental imagery [3,4], sensory processing [5,6], planning [7], attention [8,9], and language [6,10,11]. This evidence supports the view that the basal ganglia output not only targets the primary sensory-motor cortices, but also specific areas of premotor and prefrontal cortex, which include the oculomotor area of the cortex, the dorsolateral prefrontal cortex, lateral orbitofrontal cortex, and anterior cingulate/medial orbitofrontal cortices [12].…”