Single-axon tracing and three-dimensional reconstruction of centre médian-parafascicular thalamic neurons in primates

Abstract

The axonal projections from the centre median (CM)/parafascicular (Pf) thalamic complex in squirrel monkeys were studied after microiontophoretic injections of biotinylated dextran amine under electrophysiological guidance. A total of 29 axons connected to their parent cell body were entirely reconstructed from serial sections with a camera lucida. Our investigation shows that the CM and Pf nuclei in primates comprise three types of projection neurons: (1) neurons that innervate densely and focally the striatum; (2) neurons that arborize diffusely in the cerebral cortex; and (3) neurons that innervate both striatum and cerebral cortex. Striatal innervation of CM origin consists of dense clusters of axon terminals exhibiting pedunculated varicosities and forming oblique bands in the dorsolateral sector of putamen (sensorimotor striatal territory). The same type of striatal innervation occurs in the head of caudate nucleus (associative striatal territory) in cases of Pf-labeled neurons. The CM neurons that target cerebral cortex arborize principally in motor and premotor areas, whereas Pf neurons innervate chiefly prefrontal areas. Cortical innervation from both nuclei is much more profuse in layers V and VI than in layer I. Our three-dimensional reconstruction studies show that dendritic and axonal arborizations of CM neurons extend essentially along the sagittal plane. These results revealed that, in contrast to rodents where virtually all Pf neurons project to both striatum and cortex, the primate CM/Pf complex harbors several types of highly patterned projection neurons. As such, this complex might be considered as an integral part of the widely distributed basal ganglia neuronal system.

Novel and Distinct Operational Principles of Intralaminar Thalamic Neurons and Their Striatal Projections

“…The dendrites of CL neurons adhered to the bushy architecture typical of thalamic relay neurons, whereas the dendrites of Pf neurons were reticular-like, in agreement with previous studies (Scheibel and Scheibel, 1967;Jones, 1985;Sugiyama et al, 1992;Deschênes et al, 1996a,b;Parent and Parent, 2005). The distinct firing properties of CL and Pf neurons in vivo might reflect these conspicuously different dendritic arbors.…”

Postnatal maturational properties of rat parafascicular thalamic neurons recorded in vitro

“…The morphology of the biocytin-labeled Pf cells sampled in this study matched that previously reported for Pf cells in rodents and other species using various single cell labeling techniques (Hazlett et al, 1976;Sugiyama et al, 1992b;Fenelon et al, 1994;Deschenes et al, 1995;Deschenes et al, 1996;Vercelli et al, 2003;Parent and Parent, 2005). Specifically, Pf cells exhibited long, unramifying primary dendrites unlike the compact, bushy dendritic trees which characterize neighboring thalamic relay neurons in the rat (Harris, 1986;Sawyer et al, 1989;Bartlett and Smith, 1999;Li et al, 2003).…”

“…In contrast, anatomical studies have long recognized that many cells in the Pf have a distinct morphology compared with thalamic relay nuclei (Hazlett et al, 1976;Hazlett and Hazlett, 1977;Pearson et al, 1984;Parent and Parent, 2005). Typically, they contain long unbranching processes in their proximal dendritic trees.…”

In vivo evidence for the selective subcortical degeneration in Huntington's disease

“…As the centro-median thalamic nucleus, sending back its efferents to the sensorimotor territories of the striatum and to the motor and premotor cortical areas, is predominantly involved in the motor basal ganglia-thalamocortical loop (Alexander et al, 1990;Parent and Parent, 2005), this altogether suggests that the motor subcortical loop is the most affected by the degenerative process at this stage of the disease.…”