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.

Figure 1. Common motor infrastructure from lamprey to man

Basic patterns of motor behaviour are controlled by neuronal networks (CPGs) located in the brainstem (e.g. swallowing, breathing) or the spinal cord (e.g. locomotion) (indicated as yellow circles), and the organisation is very similar throughout vertebrate phylogeny. The organisation of the basal ganglia is conserved from lamprey to primates. The basal ganglia control the activity in different brainstem motor centres and play a crucial role in the selection of motor behaviours. In primates and man a well-developed cerebral cortex provides a locus for networks controlling fine motor skills, and it also receives input from the basal ganglia via the thalamus.

Figure 2. The organisation of the basal ganglia is almost identical throughout vertebrate phylogeny – from lamprey to primates

A, the striatum consists of GABAergic neurones (blue), as also globus pallidus externa (GPe), globus pallidus interna (GPi) and substantia nigra pars reticulata (SNr). SNr and GPi represent the output level of the basal ganglia, and it projects via different subpopulations of neurones to tectum (superior colliculus), the mesencephalic (MLR) and diencephalic (DLR) locomotor command regions and other brainstem motor centres, and also back to thalamus and cortex (pallium in lower vertebrates). The indirect loop is represented by the GPe, the subthalamic nucleus (STN) and the output level (SNr/GPi). The striatal neurones of the direct pathway to SNr/GPi express D1R and substance P (D1/SP), while the indirect pathway neurones in striatum express D2R and enkephalin (D2/Enk). Excitatory glutamatergic neurones are in pink. Also indicated is the dopamine supply from the substantia nigra pars compacta (SNc; green). B, the vertebrate lineage is represented. The lamprey had already diverged from the main vertebrate line 560 million years ago (mya); mammals emerged only some 130 mya and humans some 0.2 mya. Yet the design of the basal ganglia is conserved from lamprey to primates. In mammals there is a well-described pallido-thalamo-cortico projection that has not yet been investigated in the lamprey.

Figure 3. Conceptual scheme of a modular organisation of the basal ganglia, with one module for each type of motor programme

Each module would contain the D1R and D2R projection neurones and the components of the direct and indirect pathway GPi, SNr, GPe and STN (see Fig. 2A). Each module would be activated, if sufficient drive occurs from neurones in pallium/cortex and thalamus. The responsiveness of the modules would be determined by the tonic dopaminergic drive. Whereas the lamprey would have a limited behavioural repertoire and few modules, mammals and particularly primates have a very varied and versatile motor repertoire and presumably a greater number of modules.