Interactions between the Midbrain Superior Colliculus and the Basal Ganglia

Abstract

An important component of the architecture of cortico-basal ganglia connections is the parallel, re-entrant looped projections that originate and return to specific regions of the cerebral cortex. However, such loops are unlikely to have been the first evolutionary example of a closed-loop architecture involving the basal ganglia. A phylogenetically older, series of subcortical loops can be shown to link the basal ganglia with many brainstem sensorimotor structures. While the characteristics of individual components of potential subcortical re-entrant loops have been documented, the full extent to which they represent functionally segregated parallel projecting channels remains to be determined. However, for one midbrain structure, the superior colliculus (SC), anatomical evidence for closed-loop connectivity with the basal ganglia is robust, and can serve as an example against which the loop hypothesis can be evaluated for other subcortical structures. Examination of ascending projections from the SC to the thalamus suggests there may be multiple functionally segregated systems. The SC also provides afferent signals to the other principal input nuclei of the basal ganglia, the dopaminergic neurones in substantia nigra and to the subthalamic nucleus. Recent electrophysiological investigations show that the afferent signals originating in the SC carry important information concerning the onset of biologically significant events to each of the basal ganglia input nuclei. Such signals are widely regarded as crucial for the proposed functions of selection and reinforcement learning with which the basal ganglia have so often been associated.

Keywords: dopamine; reinforcement learning; selection; striatum; substantia nigra; subthalamus; superior colliculus; thalamus.

Figure 1

Cortical and subcortical sensorimotor loops through the basal ganglia (modified with permission from McHaffie et al. , 2005). (A) The position of the thalamic relay is on the return arm of cortical loops, while for subcortical loops, the thalamic relay is on the input side. (B) Predominantly excitatory regions and connections are in red; inhibitory regions and connections are in blue. GPi, internal globus pallidus; SN, substantia nigra; Thal, thalamus.

Figure 2

The tecto-thalamo-striatal projection. Thalamo-striatal neurones in the central medial nucleus of the thalamus labeled with CTb (purple) retrogradely transported from the striatum, surrounded by terminal boutons labeled with biotinylated dextran (brown) anterogradely transported from the deep layers of the superior colliculus.

Figure 3

The tecto-subthalamic and tecto-nigral projections in rat (modified with permission from Coizet et al. , 2009). A large injection of the anterograde tracer PHA-L into the deep layers of the lateral superior colliculus (SC) produced dense fiber and terminal labeling in substantia nigra pars compacta (SNc) and subthalamic nucleus (STN). Note the dense clusters of terminal boutons, presumably surrounding neuronal cell bodies in STN (see inset). The tecto-thalamic projection was also confirmed in this case with terminal labeling evident in the parafasicular thalamic nucleus (PF). ic, Internal capsule; SNr, substantia nigra pars reticulate; ZI, zona incerta.

Figure 4

A schematic illustration of the proposed convergence of short-latency phasic inputs to the striatum elicited by an unpredicted visual event. Direct retinal input to the superior colliculus could be re-directed, via branched projections to the intralaminar thalamic nuclei and to the substantia nigra pars compacta. At present, the identities of the neurotransmitters used in branched connections from the superior colliclus are unknown. Consequent, potentially converging phasic inputs to the striatum from intralaminar nuclei (GLU, glutamate) and substantia nigra (DA, dopamine) are likely to play a critical role in reinforcement learning.