Reticulospinal neurons in the pontomedullary reticular formation of the monkey (Macaca fascicularis)

Department of Psychology and Neuroscience Program, Michigan State University, East Lansing, MI 48824, USA.
Neuroscience (Impact Factor: 3.36). 08/2009; 163(4):1158-70. DOI: 10.1016/j.neuroscience.2009.07.036
Source: PubMed


Recent neurophysiological studies indicate a role for reticulospinal neurons of the pontomedullary reticular formation (PMRF) in motor preparation and goal-directed reaching in the monkey. Although the macaque monkey is an important model for such investigations, little is known regarding the organization of the PMRF in the monkey. In the present study, we investigated the distribution of reticulospinal neurons in the macaque. Bilateral injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were made into the cervical spinal cord. A wide band of retrogradely labeled cells was found in the gigantocellular reticular nucleus (Gi) and labeled cells continued rostrally into the caudal pontine reticular nucleus (PnC) and into the oral pontine reticular nucleus (PnO). Additional retrograde tracing studies following unilateral cervical spinal cord injections of cholera toxin subunit B revealed that there were more ipsilateral (60%) than contralateral (40%) projecting cells in Gi, while an approximately 50:50 ratio contralateral to ipsilateral split was found in PnC and more contralateral projections arose from PnO. Reticulospinal neurons in PMRF ranged widely in size from over 50 microm to under 25 microm across the major somatic axis. Labeled giant cells (soma diameters greater than 50 microm) comprised a small percentage of the neurons and were found in Gi, PnC and PnO. The present results define the origins of the reticulospinal system in the monkey and provide an important foundation for future investigations of the anatomy and physiology of this system in primates.

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    • "The gigantocellular reticular formation is well known for its importance in behavioral arousal (Morest and Sutin 1961; Steriade et al. 1984; Boissard et al. 2002; Luppi et al. 2011), pain modulation (Nagata et al. 2003; Mason 2005), and motor modulation (Winson 1981; Robinson et al. 1994; Li et al. 1996; Fay and Norgren 1997; Tellegen and Dubbeldam 1999; Mileykovskiy et al. 2000; Hattox et al. 2002) through its connections with other parts of the central nervous system. Among them, the spinal cord is one of the major targets of efferents from the gigantocellular reticular formation (Peterson et al. 1979; Martin et al. 1985; Holstege and Kuypers 1982; Zagon and Bacon 1991; Zou et al. 1996; Hermann et al. 2003; Lefler et al. 2008; Reed et al. 2008; Sakai et al. 2009; Liang et al. 2011). It has been reported that fibers from the gigantocellular reticular formation travel in both the lateral and the ventral funiculi in the white matter of the spinal cord and terminate in laminae 7 and 8 in rats and other large animals (Nyberg-Hansen 1965; Petras 1967; Jones and Yang 1985; Mitani et al. 1988; Hermann et al. 2003). "
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    ABSTRACT: The present study investigated the projections of the gigantocellular reticular nucleus (Gi) and its neighbors-the dorsal paragigantocellular reticular nucleus (DPGi), the alpha/ventral part of the gigantocellular reticular nucleus (GiA/V), and the lateral paragigantocellular reticular nucleus (LPGi)-to the mouse spinal cord by injecting the anterograde tracer biotinylated dextran amine (BDA) into the Gi, DPGi, GiA/GiV, and LPGi. The Gi projected to the entire spinal cord bilaterally with an ipsilateral predominance. Its fibers traveled in both the ventral and lateral funiculi with a greater presence in the ventral funiculus. As the fibers descended in the spinal cord, their density in the lateral funiculus increased. The terminals were present mainly in laminae 7-10 with a dorsolateral expansion caudally. In the lumbar and sacral cord, a considerable number of terminals were also present in laminae 5 and 6. Contralateral fibers shared a similar pattern to their ipsilateral counterparts and some fibers were seen to cross the midline. Fibers arising from the DPGi were similarly distributed in the spinal cord except that there was no dorsolateral expansion in the lumbar and sacral segments and there were fewer fiber terminals. Fibers arising from GiA/V predominantly traveled in the ventral and lateral funiculi ipsilaterally. Ipsilaterally, the density of fibers in the ventral funiculus decreased along the rostrocaudal axis, whereas the density of fibers in the lateral funiculus increased. They terminate mainly in the medial ventral horn and lamina 10 with a smaller number of fibers in the dorsal horn. Fibers arising from the LPGi traveled in both the ventral and lateral funiculi and the density of these fibers in the ventral and lateral funiculi decreased dramatically in the lumbar and sacral segments. Their terminals were present in the ventral horn with a large portion of them terminating in the motor neuron columns. The present study is the first demonstration of the termination pattern of fibers arising from the Gi, DPGi, GiA/GiV, and LPGi in the mouse spinal cord. It provides an anatomical foundation for those who are conducting spinal cord injury and locomotion related research.
    Full-text · Article · Jan 2015 · Brain Structure and Function
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    • "While the corticospinal tract offers the most direct access to the spinal cord, the corticobular pathway connecting through the reticular formation provides an alternative pathway (Lemon 2008). While the reticulospinal tract has well-established role in posture and locomotion (Deliagina et al. 2008; Honeycutt et al. 2009; Honeycutt and Nichols 2010; Mori 1987; Mori et al. 1989; Musienko et al. 2008; Schepens et al. 2008; Stapley and Drew 2009), new evidence expands this traditional view highlighting its role during voluntary movements like reaching (Buford and Davidson 2004; Davidson et al. 2007; Sakai et al. 2009). Although this type of task is known to also be mediated by corticospinal pathways, recordings from the reticular formation demonstrate that these cells are strongly modulated during reaching. "
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    ABSTRACT: The reticulospinal tract was recently shown to have synaptic connections to the intrinsic muscles of the fingers in non-human primates, indicating it may contribute to hand function long thought to be controlled exclusively through corticospinal pathways. Our objective was to obtain evidence supporting the hypothesis that these same anatomical connections exist in humans. StartReact, an involuntary release of a planned movement via the startle reflex, provides a non-invasive means to examine the reticulospinal tract in humans. We found that startReact was triggered during coordinated grasp but not individuated finger movements. This result suggests that the reticulospinal tract does have connections to the intrinsic muscles of the fingers in humans but its functional role is limited to coordinated movement of the whole hand. These results do not diminish the well-established role of corticospinal pathways in the control of hand movement. Indeed, they cement the significance of corticospinal pathways in individuated finger movement control. Still, these results point to an updated and expanded view of distal hand control where reticulospinal and corticospinal pathways work in parallel to generate a large repertoire of diverse, coordinated movement in the hand. Finally, the presence of reticulospinal pathways to the muscles of the hand makes this pathway an attractive therapeutic target for clinical populations where the corticospinal tract is absent or injured.
    Full-text · Article · Jul 2013 · Journal of Neurophysiology
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    • "The reticulospinal tract is a brain stem pathway that originates in the gigantocellular reticular nucleus (lateral/medullary reticulospinal tract) and caudal and oral pontine reticular nuclei (medial/ pontine reticulospinal tract) and descends in the brain stem both bilaterally and uncrossed, respectively (Kuypers 1964). Both tracts terminate in spinal gray matter bilaterally with minimal ipsilateral predominance (Sakai et al. 2009) across multiple spinal segments (Matsuyama et al. 1997). "
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    ABSTRACT: The effect of reticular formation excitability on maximum voluntary torque (MVT) generation and associated muscle activation at the shoulder and elbow was investigated through natural elicitation (active head rotation) of the asymmetric tonic neck reflex (ATNR) in 26 individuals with stroke and 9 age-range-matched controls. Isometric MVT generation at the shoulder and elbow was quantified with the head rotated (face pointing) contralateral and ipsilateral to the paretic (stroke) and dominant (control) arm. Given the dominance of abnormal torque coupling of elbow flexion with shoulder abduction (flexion synergy) in stroke and well developed animal models demonstrating a linkage between reticular formation and ipsilateral elbow flexors and shoulder abductors, we hypothesized that constituent torques of flexion synergy, specifically elbow flexion and shoulder abduction, would increase with contralateral head rotation. The findings of this investigation support this hypothesis. Increases in MVT for 3 out of 4 flexion synergy constituents (elbow flexion, shoulder abduction, and shoulder external rotation) were observed during contralateral head rotation only in individuals with stroke. EMG data of the associated muscle co-activations were non-significant however are presented for consideration in light of a likely underpowered statistical design for this specific variable. This study provides evidence for not only the re-emergence of ATNR following stroke, but also indicates a common neuroanatomical link, namely an increased reliance on ipsilateral reticulospinal pathways, as the likely mechanism underlying the expression of both ATNR and flexion synergy that results in the loss of independent joint control.
    Full-text · Article · Sep 2012 · Journal of Neurophysiology
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