The cortico-basal ganglia integrative network: the role of the thalamus

Abstract

The thalamus is a critical component of the frontal cortical-basal ganglia-thalamic circuits that mediate motivation and emotional drive, planning and cognition for the development and expression of goal-directed behaviors. Each functional region of the frontal cortex is connected with specific areas of each basal ganglia (BG) structure and of the thalamus. In addition, the thalamus sends a massive, topographically organized projection directly to the striatum. Tract-tracing and physiological experiments have indicated a general topographic organization of the cortical-BG-thalamic loops and supported a model of BG function based on parallel and segregated pathways. However, the learning and execution of appropriate behavioral responses require integration of inputs related to emotional, cognitive, and motor cortical functions. Our recent data indicate that integration may occur via non-reciprocal connections between the striatum and substantia nigra and within "hot spots" of convergence between corticostriatal projections from different functional regions. Similarly, integration may exist in the thalamus. There are non-reciprocal connections between the thalamus and cortex via thalamocortical projections that terminate in the superficial and deep cortical layers. These terminals can influence different functional cortical areas that, in turn, project to the striatum and back to the thalamus. In addition, a non-reciprocal corticothalamic projection terminates in thalamic regions that are parts of other circuits. Finally, 'hot spots' of convergence between terminals from different cortical regions may also occur in the thalamus as is seen in the striatum. Thus, via several different pathways, the thalamus may serve as an important center of integration of networks that underlie the ability to modulate behaviors.

Fig. 1

Diagram illustrates functionally similar cortical and thalamic regions projection to the same striatal area. Note the cortico-thalamic projection is reciprocal. The caudal motor-related areas of the frontal lobe (primary motor area, M1; caudal premotor cortex, PMc; supplementary motor area, SMA; and caudal cingulate motor area, CMAc) are primarily connected with the ventral thalamic nuclei VPLo and VLo. These cortical and thalamic regions send converging efferents projections to the dorsolateral and dorsocentral putamen. In contrast, the rostral motor-related areas of the frontal lobe (rostral premotor cortex, PMr; pre-supplementary motor area, PreSMA; and rostral cingulate motor area, CMAr) are primarily connected with the ventral thalamic nucleus VApc. These cortical areas and the VApc send converging efferents projections to the dorsolateral caudate nucleus and to the rostral putamen. Both rostral and caudal premotor areas, and CMAc are connected with the ventral thalamic nucleus VLc. These cortical areas and the VLc send efferents projections to the dorsolateral caudate n.

Fig. 2

Summary of thalamic terminal organization in cortical layers. Projections to the deep layers may interact with neurons that, in turn, project back to both the thalamus and striatum. These terminals can directly reinforce corticothalamic and corticostriatal inputs to specific cortico-BG circuits (A). In addition, through the non-reciprocal corticothalamic projection, terminals in layer V may also interface with other cortico-BG circuits via projection to a thalamic region that is part of another circuit system (B). Thalamocortical projections to the superficial layers may have a similar dual function. These projections may interact with the apical dendrites of layer V cells, further reinforcing each parallel circuit. In addition, through corticocortical projections from layer III, these terminals may influence adjacent circuits (modified from J. Neurosci., 2002, 22:8117–8132).