The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated

Abstract

Anatomical findings in primates and rodents have led to a description of several parallel segregated basal ganglia-thalamocortical circuits leading from a distinct frontocortical area, via separate regions in the basal ganglia and the thalamus, back to the frontocortical area from which the circuit originates. One of the questions raised by the concept of parallelism is whether and how the different circuits interact. The present Commentary proposes that interaction is inherent in the neural architecture of the basal ganglia-thalamocortical circuits. This proposal is based on the re-examination of the data on the topographical organization of the frontocortical-basal ganglia connections which indicates that each circuit-engaged striatal region sends divergent projections to parts of both substantia nigra pars reticulata and the internal segment of the globus pallidus (each ventral striatal region sends divergent projections to parts of ventral pallidum, substantia nigra pars reticulata and globus pallidus), and this segregation is maintained at subsequent thalamic and frontocortical levels. This results in an asymmetry in the frontal cortex-basal ganglia relationships, so that while each frontocortical subfield innervates one striatal region, each striatal region influences the basal ganglia output to two frontocortical subfields. Because of this asymmetry, at least one of the frontocortical targets of a given circuit-engaged striatal region is not the source of its frontocortical input. Since this organization is inconsistent with an arrangement in closed segregated circuits we introduce the concept of a “split circuit”. A split circuit emanates from one frontocortical area, but terminates in two frontocortical areas. Thus, a split circuit contains at least one “open” striato-fronto-cortical pathway, that leads from a circuit-engaged striatal region to a frontocortical area which is a source of a different circuit. In this manner split circuits are interconnected via their open pathways. The second striato-fronto-cortical pathway of a split circuit can be another open pathway, or it can re-enter the frontocortical area of origin, forming a closed circuit. On the basis of the available anatomical data we tentatively identified a motor, an associative, and a limbic split circuit, each containing a closed circuit and an open pathway. The motor split circuit contains a closed motor circuit that re-enters the motor and premotor cortical areas and an open motor pathway that terminates in the associative prefrontal cortex. The associative split circuit contains a closed associative circuit that re-enters the associative prefrontal cortex and an open associative pathway that terminates in the premotor cortex. The limbic split circuit contains a closed limbic circuit that re-enters the limbic prefrontal cortex, an open limbic pathway that terminates in the associative prefrontal cortex, and possibly an additional open limbic pathway terminating in the motor/premotor cortices. Possible functional implications of this open interconnected organization of the basal ganglia-thalamocortical circuits are discussed.