Distribution of Motor Cortical Neuron Synaptic Terminals on Monkey Parvocellular Red Nucleus Neurons

Jenny, Arthur B.; Smith, J L; Bernardo, Kerry L.; Woolsey, Thomas A.

doi:10.3109/08990229109144726

Cited by 6 publications

(8 citation statements)

References 23 publications

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“…It has also been reported in recent work in the turtle (Keifer et al, 1992) and for cortically mediated inhibition of rubral neurons in the cat (Katsumaru et al, 1984) and has been demonstrated with immuno-GABA-gold labeling in RNm in the monkey (Ralston and Milroy, 1992). In a brief electron microscopic study of corticorubral terminals in RNp of one monkey (Jenny et al, 1991), the authors described cortical terminals synapsing upon proximal and distal dendrites of rubral neurons. These authors did not use GABA immunohistochemistry and depicted one cortical axodendritic terminal containing rounded synaptic vesicles but did not report the presence of glomerular relationships of cortical afFerents with dendritic spines, small-diameter dendrites, or psds that are such a prominent finding of the present study.…”

Section: The Cortical Projection and Its Relationship With Local Circsupporting

confidence: 53%

“…These authors did not use GABA immunohistochemistry and depicted one cortical axodendritic terminal containing rounded synaptic vesicles but did not report the presence of glomerular relationships of cortical afFerents with dendritic spines, small-diameter dendrites, or psds that are such a prominent finding of the present study. This discrepancy may be explained by the fact that most interactions of cortical afferents with local circuit neurons take place at the distal dendrites of projection neurons, and Jenny et al (1991) described cortical terminals that were more proximally located.…”

Section: The Cortical Projection and Its Relationship With Local Circmentioning

confidence: 99%

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Corticorubral synaptic organization in Macaca fascicularis: A study utilizing degeneration, anterograde transport of WGA‐HRP, and combined immuno‐GABA‐gold technique and computer‐assisted reconstruction

Ralston

1994

J of Comparative Neurology

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The macaque red nucleus receives afferents from two major sources, the cerebral cortex and the deep cerebellar nuclei. Approximately 90% of the corticorubral afferent axons project to pars parvicellularis of the red nucleus, the neurons of which transmit information to the cerebellum by way of the inferior olivary nucleus. The remaining 10% project to pars magnocellularis of the red nucleus, the major projection of which is to the spinal cord. In this study, corticorubral terminations labeled following lesions or injections of wheatgerm agglutinin conjugated to horseradish-peroxidase into the topographically defined hand area of the primary motor cortex were quantitatively studied via electron microscopy. Cortical afferent terminals within pars parvicellularis and pars magnocellularis synapse upon all regions of the dendritic arbors of rubral projection neurons. However, the majority of these labeled afferents synapse upon thin-diameter shafts or presumed spinous processes of rubral distal dendrites as well as upon vesicle-containing profiles of presynaptic dendrites of local circuit interneurons that are gamma-aminobutyric acid-immunoreactive, as identified by postembedding immunohistochemistry. Synaptic contacts formed by the labeled cortical terminal were large in width and extended through several serial sections. Synaptic contacts formed by the presynaptic dendritic profiles, on the other hand, were more punctate and could be seen in only one or two serial sections. These latter synaptic interactions probably provide a modification of the effects of cortical input to rubral projection neurons as suggested by previous physiological studies that indicated the dominance of cortical input onto distal dendrites as well as involvement with inhibitory circuits. An example of the complexities of these synaptic interactions is further demonstrated by a three-dimensional computer reconstruction. This quantitative study of corticorubral afferents in the macaque monkey provides insight into the interactions of cerebral cortical afferents with rubral projection neurons and their relationship with local circuit inhibitory interneurons to elucidate the role played by the cortex in the activation of rubral neurons.

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Section: The Cortical Projection and Its Relationship With Local Circsupporting

confidence: 53%

Section: The Cortical Projection and Its Relationship With Local Circmentioning

confidence: 99%

Corticorubral synaptic organization in Macaca fascicularis: A study utilizing degeneration, anterograde transport of WGA‐HRP, and combined immuno‐GABA‐gold technique and computer‐assisted reconstruction

Ralston

1994

J of Comparative Neurology

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“…Thus, given the cellular distribution of our sample of boutons in the rat, it appears that the more distally located dendritic arbors of rubrospinal neurons receive overlapping inputs from the cerebellum and cerebral cortex, whereas the soma and the most proximally located dendrites receive the cerebellar inputs. This partly overlapping organization of cerebellar and cortical inputs may be similar to that described in monkeys (Jenny et al, 1991; Ralston, 1994a,b) and should be reexamined in other mammals. The cellular localization of the hypothalamorubral projections has not been described previously in any species.…”

Section: Discussionsupporting

confidence: 77%

Comparison of cortically and subcortically controlled motor systems. II. distribution of anterogradely labeled terminal boutons on intracellularly filled rubrospinal neurons in rat and turtle

Keifer

Lustig

2000

J. Comp. Neurol.

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The present study examined the circuitry of the red nucleus of the Sprague‐Dawley rat and the freshwater pond turtle, Chrysemys picta, by using intracellular cell filling combined with anterograde tract tracing. Although both species have a well‐developed cerebellorubral system, they differ in that the red nucleus of rats receives direct input from the motor areas of the cerebral cortex, whereas turtles do not. However, a direct descending projection from the hypothalamus to the red nucleus of turtles has been described. The aim of this study was to elucidate the relative functional contributions of the cerebellum and descending inputs to motor signal generation in the red nucleus. The results show that the cellular distribution of cerebellar inputs on rubrospinal neurons is similar between the rat and turtle; these projections are observed on the soma and the proximal and distal dendrites. In contrast, the hypothalamic inputs in turtles occupy mainly the more distally located dendrites, similar to the position of the cortical inputs in rats. These findings suggest that, first, the cerebellar inputs are not spatially segregated from the cortical or hypothalamic inputs in rats or turtles, as far as can be determined by light microscopy. Second, there is specificity of input from the cortex in rats and hypothalamus in turtles onto the distal portions of the dendrites. The similarity in the organizational features of the mammalian and non‐mammalian cerebellorubrospinal systems has implications for interpretations of the relative roles of the cerebellum and cerebral cortex in motor control. J. Comp. Neurol. 416:101–111, 2000. © 2000 Wiley‐Liss, Inc.

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“…The mammalian red nucleus (RN) processes sensorimotor information from the frontoparietal cortex (Kuypers and Lawrence, 1967; von Monakow et al, 1979; Humphrey et al, 1984; Jenny et al, 1991; Ralston, 1994a; Tokuno et al, 1995; Burman et al, 2000) and the cerebellar cortex (Flumenfelt et al, 1973; Miller and Strominger, 1977; Stanton, 1980; Asanuma et al, 1983; Ralston, 1994a). It transmits the transformed signals back to the cerebellum through the rubroolivary projection to the climbing fiber system (De Zeeuw et al, 1998) and also to the spinal cord through the rubrospinal neuron populations (Eccles et al, 1967; Massion, 1967; Ralston et al, 1988; Keifer and Houk, 1994).…”

mentioning

confidence: 99%

Geometry of rubrospinal, rubroolivary, and local circuit neurons in the macaque red nucleus

Burman

Darian‐Smith

2000

J. Comp. Neurol.

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The primate red nucleus consists of three main neuron subpopulations, namely, rubrospinal neurons in the magnocellular nucleus, rubroolivary cells in the parvocellular nucleus, and local circuit neurons in both subnuclei: Each subpopulation has unique cerebellar and neocortical inputs. The structural framework for the interactions of these rubral subpopulations remains poorly defined and was the focus of this study in six macaques. Somata of rubrospinal neurons, dorsolateral-spinal (DL-spinal) neurons, as defined in the accompanying paper (Burman et al. [2000] J. Comp. Neurol., this issue), and rubroolivary neurons were labeled retrogradely first with Fast Blue injected either into the cervical spinal cord or the inferior olive. The soma/dendrite profiles of selected cells (53 rubrospinal, 19 DL-spinal, and 17 rubroolivary cells) were visualized by the intracellular injection of Lucifer Yellow/biocytin in fixed slices (400 microm thick) of midbrain. The descriptive statistics of the somata and the dendritic arborization of each rubral neuron type were established. Projection neuron subpopulations had similar but differentiable soma/dendrite profiles, with four to six slender, spine-bearing dendritic trees radiating out approximately 400 microm from the soma. Twelve presumed interneurons, all in the parvocellular nucleus, differed from projection neurons in that they had smaller somata and many slender, spine-bearing segments that constituted the multibranching dendrite profile that radiated out approximately 250 microm from the soma. A tentative model of the macaque rubral microcircuitry was developed, and its functional implications were explored. It incorporated 1) the known topography of the nucleus and its connections, 2) our data specifying the soma/dendrite morphology of the three main rubral neuron types, and 3) the ultrastructure reported by other laboratories of intrarubral synaptic connections.

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Distribution of Motor Cortical Neuron Synaptic Terminals on Monkey Parvocellular Red Nucleus Neurons

Cited by 6 publications

References 23 publications

Corticorubral synaptic organization in Macaca fascicularis: A study utilizing degeneration, anterograde transport of WGA‐HRP, and combined immuno‐GABA‐gold technique and computer‐assisted reconstruction

Corticorubral synaptic organization in Macaca fascicularis: A study utilizing degeneration, anterograde transport of WGA‐HRP, and combined immuno‐GABA‐gold technique and computer‐assisted reconstruction

Comparison of cortically and subcortically controlled motor systems. II. distribution of anterogradely labeled terminal boutons on intracellularly filled rubrospinal neurons in rat and turtle

Geometry of rubrospinal, rubroolivary, and local circuit neurons in the macaque red nucleus

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