The evolutionary origin of the vertebrate basal ganglia and its role in action selection

Abstract

The group of nuclei within the basal ganglia of the forebrain is central to the control of movement. We present data showing that the structure and function of the basal ganglia have been conserved throughout vertebrate evolution over some 560 million years. The interaction between the different nuclei within the basal ganglia is conserved as well as the cellular and synaptic properties and transmitters. We consider the role of the conserved basal ganglia circuitry for basic patterns of motor behaviour controlled via brainstem circuits. The output of the basal ganglia consists of tonically active GABAergic neurones, which target brainstem motor centres responsible for different patterns of behaviour, such as eye and locomotor movements, posture, and feeding. A prerequisite for activating or releasing a motor programme is that this GABAergic inhibition is temporarily reduced. This can be achieved through activation of GABAergic projection neurons from striatum, the input level of the basal ganglia, given an appropriate synaptic drive from cortex, thalamus and the dopamine system. The tonic inhibition of the motor centres at rest most likely serves to prevent the different motor programmes from becoming active when not intended. Striatal projection neurones are subdivided into one group with dopamine 1 receptors that provides increased excitability of the direct pathway that can initiate movements, while inhibitory dopamine 2 receptors are expressed on neurones that instead inhibit movements and are part of the 'indirect loop' in mammals as well as lamprey. We review the evidence showing that all basic features of the basal ganglia have been conserved throughout vertebrate phylogeny, and discuss these findings in relation to the role of the basal ganglia in selection of behaviour.

Midbrain circuits that set locomotor speed and gait selection

“…As previously shown, PPN neurons receive rich projection from basal ganglia nuclei 12,14 , but also from many midbrain and medullary sensory-motor nuclei as well as from motor cortex. This innervation pattern is in accordance with a role of glutamatergic PPN neurons for exploratory locomotor behaviour under the motor action selection of the basal ganglia 30,31,32,33,34,7 . The strong connection from the basal ganglia also suggests that dysregulation of glutamatergic neurons in PPN may play important roles in Parkinson’s disease related locomotor disability.…”

Deep Brain Stimulation for Movement Disorders of Basal Ganglia Origin: Restoring Function or Functionality?

“…The role of the basal ganglia in action selection has been long considered to be one of the fundamental roles of these nuclei [23]. It is most often used in the sense that the basal ganglia play a role in making the most appropriate action for a given situation by selecting the optimal response and blocking competing ones [24].…”

“…The absence of overt motor impairments with surgical disruption of basal ganglia output in patients with movement disorders does not negate a more significant function of the basal ganglia under normal conditions. The fact that the basal ganglia can be identified at the earliest stages in vertebrate evolution and that the evolutionary expansion of these structures mirrors that of the cerebral cortex is indirect evidence for their biological importance [23,321]. However, the Bparadox^suggests that the contribution of the basal ganglia to movement may be largely assistive rather than essential, and that its loss can be compensated for by the system as a whole with little deficit.…”

A descending dopamine pathway conserved from basal vertebrates to mammals

“…A growing body of evidence supports the view that basal ganglia connectivity is highly conserved among vertebrates, from lampreys to mammals (9-11; for review, see ref. 12), with some interspecies differences recently highlighted (13). As such, the homology between DA cell populations remains to be resolved in vertebrates.…”