The Basal Ganglia Downstream Control of Action - An Evolutionarily Conserved Strategy

Abstract

The motor areas of the cortex and the basal ganglia both contribute to determining which motor actions will be recruited at any moment in time, and their functions are intertwined. Here, we review the basal ganglia mechanisms underlying the selection of behavior of the downstream control of motor centers in the midbrain and brainstem and show that the basic organization of the forebrain motor system is evolutionarily conserved throughout vertebrate phylogeny. The output level of the basal ganglia (e.g. substantia nigra pars reticulata) has GABAergic neurons that are spontaneously active at rest and inhibit a number of specific motor centers, each of which can be relieved from inhibition if the inhibitory output neurons themselves become inhibited. The motor areas of the cortex act partially via the dorsolateral striatum (putamen), which has specific modules for the forelimb, hindlimb, trunk, etc. Each module operates in turn through the two types of striatal projection neurons that control the output modules of the basal ganglia and thereby the downstream motor centers. The mechanisms for lateral inhibition in the striatum are reviewed as well as other striatal mechanisms contributing to action selection. The motor cortex also exerts a direct excitatory action on specific motor centers. An overview is given of the basal ganglia control exerted on the different midbrain/brainstem motor centers, and the efference copy information fed back via the thalamus to the striatum and cortex, which is of importance for the planning of future movements.

Keywords: Evolution; basal ganglia; corticostriatal; dorsolateral striatum; motor centers; striatonigral.; substantia nigra pars reticulata.

Fig. (1)

The basic organization of the lamprey and the mammalian basal ganglia is similar. (A) The general diagram of the basal ganglia applies to both lamprey and mammals. The striatum consists of GABAergic neurons, as do globus pallidus pars externa (GPe), globus pallidus pars interna (GPi) and substantia nigra pars reticulata (SNr). SNr and GPi represent the output level of the basal ganglia, and they project via different subpopulations of neurons to the tectum/superior colliculus, the mesencephalic (MLR), and diencephalic (DLR) locomotor regions, and other brainstem motor centers, as well as back to thalamus with efference copies of information sent to the brainstem. The direct striatal projection neurons (dSPNs) that target SNr/GPi express the dopamine D1 receptor (D1) and substance P (SP), while the iSPNs (indirect striatal projection neurons) express the dopamine D2 receptor (D2) and enkephalin (Enk). Also indicated is the dopamine input from the substantia nigra pars compacta (SNc; green) to the striatum and brainstem centers. Excitatory glutamatergic neurons are shown in pink and GABAergic structures in blue. (B) A table showing the key features of the basal ganglia organization that are found in mammals and lamprey.

Fig. (2)

Modular connectivity from the motor cortex to the DLS and striatum. The modular nature of the connectivity from the different sections of the motor cortex to modules within the striatum and the connectivity via striatonigral dSPNs to modules within the SNr, which in turn each target different midbrain and brainstem motor centers. The indirect pathway via iSPNs (not illustrated) are subdivided into the same modules as the dSPNs and projects to discrete sets of GPe neurons (prototypic subsets) that in turn project to the same SNr modules as dSPNs.

Fig. (3)

Striatal microcircuit. (A) Connectivity ratio between the two types of SPNs, the fast-spiking interneurons (FS), the low threshold spiking interneurons (LTS) and the cholinergic interneurons (ChINs). Connection probabilities within and between neuronal subtypes are shown by respective arrows; numbers in red correspond to connection probabilities for a somatic pair at a distance of 50 μm, while numbers in blue correspond to 100 μm. Input from the cortex is in red and SNc is in green. (B) An SPN shown graphically with input on the most distal dendrite from other SPNs, LTS and excitatory input from the cortex and thalamus. FS targets the soma area.

Fig. (4)

Whether a cortical motor command will be efficient in activating downstream SPNs will be determined by the activity in the many concurrent input channels in the striatum. ACh, acetylcholine; DA, dopamine; GABA IN, the different GABA interneurons in the striatum; GPe arky, the arkyplallidal neurons (stop neurons), hist, histamine; PPN glu, pedunculopontine nucleus, glutamatergic part; thal, thalamus; Red, glutamatergic neurons; blue, GABAergic neuron; green, the different modulators that target SPNs.

Fig. (5)

Schematic representation of the basal ganglia downstream control of motor structures in the midbrain-brainstem with specific efference copy information transmitted back via the thalamus to cortex and striatum. Subpopulations of neurons in the cortex project to subpopulations in the striatum that in turn inhibit discrete groups of neurons in the substantia nigra pars reticulata (SNr; [19]). Each circle indicates groups of neurons. Note that the upstream axonal branches to the motor thalamus and the parafascicular nucleus (pf) forward efference copies about the specific activity in the output channels. Only the “direct pathway” connectivity between the striatum and SNr is included in this scheme. McElvain et al.’s contribution is that SNr is subdivided into subpopulations with specific motor targets and that each conveys an efference copy to different parts of the motor thalamus or pf and further to the cortex and striatum.

Fig. (6)

The connectivity of the indirect pathway and the subthalamic nucleus (STN), and activity under resting conditions and during activity in the different cell types. Under resting conditions, SPNs tend to be silent, but during bouts of behavior, they approach 40 Hz, while the neurons of the GPe (prototypic and arkypallidal), STN and SNr all have a resting level of discharge [6]. Proto, prototypic cells; thal, thalamus.