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The Journal of Neuroscience, September 15, 2002, 22(18):8117-8132
Thalamic Relay Nuclei of the Basal Ganglia Form Both Reciprocal
and Nonreciprocal Cortical Connections, Linking Multiple Frontal
Cortical Areas
Nikolaus R.
McFarland and
Suzanne N.
Haber
Department of Neurobiology and Anatomy, University of Rochester
School of Medicine and Dentistry, Rochester, New York 14642
Thalamic relay nuclei transmit basal ganglia output to the frontal
cortex, forming the last link in corticobasal ganglia circuitry. The
thalamus regulates cortical activity through differential laminar
connections, providing not only feedback, but also initiating "feedforward" loops, via nonreciprocal projections, that influence higher cortical areas. This study examines the organization of thalamic
connections with cortex from basal ganglia relay nuclei, including
ventral anterior (VA), ventral lateral (VL), and mediodorsal (MD)
nuclei, in the Macaque monkey. Anterograde and bidirectional tracer
injections ([3H]-amino acids, dextran conjugates
of Fluorescein, Lucifer Yellow or FluoroRuby, or wheat germ agglutinin)
into discrete VA/VL, MD, and frontal cortical sites demonstrate
specific thalamocortical connections. VL projections target caudal
motor areas (primary, supplementary, and caudal premotor areas),
whereas VA projections target more rostral premotor areas (including
cingulate and presupplementary motor areas) and MD projects to
dorsolateral and orbital prefrontal cortices. Thalamocortical
projections innervate cortical layers I and III, and to a lesser
extent, layer V. In motor areas layer I projections are more extensive
than those to layer III (and V). The complex laminar organization of
projections from specific thalamic sites suggests differential
regulation of cortical function. Injections of bidirectional tracers
into thalamic and frontal cortical sites also show that in comparison
to thalamocortical projections, corticothalamic projections to VA-VL
and MD are more widespread. These findings demonstrate both reciprocal
and nonreciprocal components to the thalamo-cortico-thalamic relay.
Together, these experiments indicate a dual role for VA-VL and MD
nuclei: (1) to relay basal ganglia output within specific cortical
circuits and (2) to mediate information flow between cortical circuits.
Key words:
thalamocortical; corticothalamic; ventral anterior; ventral lateral; mediodorsal; frontal cortex
Copyright © 2002 Society for Neuroscience 0270-6474/02/22188117-16$05.00/0
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