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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.(ABSTRACT TRUNCATED
AT 400 WORDS)