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A comparative neuroanatomical study of the red nucleus of the cat, macaque and human.

Onodera S, Hicks TP - PLoS ONE (2009)

Bottom Line: Myelin- and Nissl-stained sections show that a well-developed dorsomedial part of the human Nr consists of densely packed cells, deriving small myelinated fibers that continue into the medial central tegmental tract.Based on these findings we suggest there are distinct bipedal-quadrupedal differences for Nr projections to the olivary complex.The human NB may be distinguished from its more specialised ND (ND lies alongside a well-developed pNr) in the human central gray.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, School of Medicine, Iwate Medical University, Morioka, Japan. sonodera@iwate-med.ac.jp

ABSTRACT

Background: The human red nucleus (Nr) is comparatively less well-studied than that of cats or monkeys. Given the functional importance of reticular and midbrain structures in control of movement and locomotion as well as from an evolutionary perspective, we investigated the nature and extent of any differences in Nr projections to the olivary complex in quadrupedal and bipedal species. Using neuroanatomical tract-tracing techniques we developed a "neural sheet" hypothesis allowing us to propose how rubro-olivary relations differ among the three species.

Methods and findings: Wheat germ agglutinin-horseradish peroxidase staining supports findings that the cat's nucleus accessories medialis of Bechtrew (NB) projects mainly to the lateral bend of the principal olive. We clarified boundaries among nucleus of Darkschewitsch (ND), NB and parvicellular red nucleus (pNr) of the cat's neural sheet. The macaque's ND-medial accessory olivary projection is rostro-caudally organized and the dorsomedial and ventrolateral parts of the macaque's pNr may project to the principal olive's rostral and caudal dorsal lamella; in cat it projects as well to pNr. Myelin- and Nissl-stained sections show that a well-developed dorsomedial part of the human Nr consists of densely packed cells, deriving small myelinated fibers that continue into the medial central tegmental tract.

Conclusions: Based on these findings we suggest there are distinct bipedal-quadrupedal differences for Nr projections to the olivary complex. We propose the Nr of cats and monkeys comprise the ND, NB and pNr in a zonal sheet-like structure, retaining clear nuclear boundaries and an isolated, well-developed mNr. The human NB may be distinguished from its more specialised ND (ND lies alongside a well-developed pNr) in the human central gray. Phylogenetically, the NB may have been translocated into a roll-shaped Nr in the reticular formation, the dorsomedial portion of which might correspond to the cat's and monkey's NB.

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Human cerebro-cerebellar system.The medial cerebellar system receives cortical information from areas 4, 8 and 7 via the ND [62], [63], [38], [56]. The lateral cerebellar system might not have been related only to skilful motor learning via areas 4, 6, 5 and 8 [35], [36], [63], [38], [56], but also to cognitive and language processing via the prefrontal cortico-rubral projection. CTT–central tegmental tract, dD–dorsal half of cerebellar dentate nucleus, dl–dorsal lamella, Gl–cerebellar globose nucleus, lb–lateral bend, MAO–medial accessory olive, MTT–medial tegmental tract, NB–nucleus accessorius medialis of Bechterew, ND–nucleus of Darkschewitsch, pNr–parvicellular red nucleus, PO–principal olive, vD–ventral half of cerebellar dentate nucleus, vl–ventral lamella, 4–motor area, 5–somatosensory association cortex, 6–premotor area, 7–posterior parietal cortex, 8–frontal eye field, 44–Broca's speech area.
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pone-0006623-g015: Human cerebro-cerebellar system.The medial cerebellar system receives cortical information from areas 4, 8 and 7 via the ND [62], [63], [38], [56]. The lateral cerebellar system might not have been related only to skilful motor learning via areas 4, 6, 5 and 8 [35], [36], [63], [38], [56], but also to cognitive and language processing via the prefrontal cortico-rubral projection. CTT–central tegmental tract, dD–dorsal half of cerebellar dentate nucleus, dl–dorsal lamella, Gl–cerebellar globose nucleus, lb–lateral bend, MAO–medial accessory olive, MTT–medial tegmental tract, NB–nucleus accessorius medialis of Bechterew, ND–nucleus of Darkschewitsch, pNr–parvicellular red nucleus, PO–principal olive, vD–ventral half of cerebellar dentate nucleus, vl–ventral lamella, 4–motor area, 5–somatosensory association cortex, 6–premotor area, 7–posterior parietal cortex, 8–frontal eye field, 44–Broca's speech area.

Mentions: Using voxel-based morphometric analyses, Vargha-Khaden and her coworkers (2005) showed that the affected KE family members with a higher-order orofacial motor impairment during speech have significantly reduced grey matter in the inferior frontal gyrus (Broca's area), the precentral gyrus, the temporal pole, the head of the caudate nucleus and the ventral cerebellum (lobules VIIB and VIIIB) [53]. In the normal human fetus, the FOXP2 gene is expressed in not only the cerebral cortex, basal ganglia and thalamus, but also the cerebellum, inferior olivary complex and red nucleus (Lai et al., 2003 [54]; Teramitsu et al., 2004 [55]). These data propose that one circuit for FOXP2-dependent speech and language might be not only the prefronto-caudate-loop but also the inferior fronto (Broca's area)- rubro-olivo-lateral cerebellar loop. The NB may receive projections from ventral area 6, within and caudal to the inferior ramus of the arcuate sulcus (see Leichnetz et al, 1984 [56]). As this region (area F5) corresponds to human area 44 (the inferior frontal cortex) as judged through comparative architectonic analysis (Petrides and Pandya, 1994 [57]), the NB might be related to Broca's area, so it is not only the function but also the position of NB that changes between macaque and human. The present study suggests that the well-developed human NB might be related to language via its connections with Broca's area 44 (the inferior frontal cortex) and the well-developed ventral half of the cerebellar dentate nucleus (see Fig. 15), the latter which is developed more greatly than the ape's ventral half of the cerebellar dentate nucleus (see Matano, 2001 [58]). A recent diffusion tensor tractography study using MRI demonstrated that the human red nucleus receives strong projections from the prefrontal cortex (Habas and Cabanis, 2006 [59]).


A comparative neuroanatomical study of the red nucleus of the cat, macaque and human.

Onodera S, Hicks TP - PLoS ONE (2009)

Human cerebro-cerebellar system.The medial cerebellar system receives cortical information from areas 4, 8 and 7 via the ND [62], [63], [38], [56]. The lateral cerebellar system might not have been related only to skilful motor learning via areas 4, 6, 5 and 8 [35], [36], [63], [38], [56], but also to cognitive and language processing via the prefrontal cortico-rubral projection. CTT–central tegmental tract, dD–dorsal half of cerebellar dentate nucleus, dl–dorsal lamella, Gl–cerebellar globose nucleus, lb–lateral bend, MAO–medial accessory olive, MTT–medial tegmental tract, NB–nucleus accessorius medialis of Bechterew, ND–nucleus of Darkschewitsch, pNr–parvicellular red nucleus, PO–principal olive, vD–ventral half of cerebellar dentate nucleus, vl–ventral lamella, 4–motor area, 5–somatosensory association cortex, 6–premotor area, 7–posterior parietal cortex, 8–frontal eye field, 44–Broca's speech area.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2722087&req=5

pone-0006623-g015: Human cerebro-cerebellar system.The medial cerebellar system receives cortical information from areas 4, 8 and 7 via the ND [62], [63], [38], [56]. The lateral cerebellar system might not have been related only to skilful motor learning via areas 4, 6, 5 and 8 [35], [36], [63], [38], [56], but also to cognitive and language processing via the prefrontal cortico-rubral projection. CTT–central tegmental tract, dD–dorsal half of cerebellar dentate nucleus, dl–dorsal lamella, Gl–cerebellar globose nucleus, lb–lateral bend, MAO–medial accessory olive, MTT–medial tegmental tract, NB–nucleus accessorius medialis of Bechterew, ND–nucleus of Darkschewitsch, pNr–parvicellular red nucleus, PO–principal olive, vD–ventral half of cerebellar dentate nucleus, vl–ventral lamella, 4–motor area, 5–somatosensory association cortex, 6–premotor area, 7–posterior parietal cortex, 8–frontal eye field, 44–Broca's speech area.
Mentions: Using voxel-based morphometric analyses, Vargha-Khaden and her coworkers (2005) showed that the affected KE family members with a higher-order orofacial motor impairment during speech have significantly reduced grey matter in the inferior frontal gyrus (Broca's area), the precentral gyrus, the temporal pole, the head of the caudate nucleus and the ventral cerebellum (lobules VIIB and VIIIB) [53]. In the normal human fetus, the FOXP2 gene is expressed in not only the cerebral cortex, basal ganglia and thalamus, but also the cerebellum, inferior olivary complex and red nucleus (Lai et al., 2003 [54]; Teramitsu et al., 2004 [55]). These data propose that one circuit for FOXP2-dependent speech and language might be not only the prefronto-caudate-loop but also the inferior fronto (Broca's area)- rubro-olivo-lateral cerebellar loop. The NB may receive projections from ventral area 6, within and caudal to the inferior ramus of the arcuate sulcus (see Leichnetz et al, 1984 [56]). As this region (area F5) corresponds to human area 44 (the inferior frontal cortex) as judged through comparative architectonic analysis (Petrides and Pandya, 1994 [57]), the NB might be related to Broca's area, so it is not only the function but also the position of NB that changes between macaque and human. The present study suggests that the well-developed human NB might be related to language via its connections with Broca's area 44 (the inferior frontal cortex) and the well-developed ventral half of the cerebellar dentate nucleus (see Fig. 15), the latter which is developed more greatly than the ape's ventral half of the cerebellar dentate nucleus (see Matano, 2001 [58]). A recent diffusion tensor tractography study using MRI demonstrated that the human red nucleus receives strong projections from the prefrontal cortex (Habas and Cabanis, 2006 [59]).

Bottom Line: Myelin- and Nissl-stained sections show that a well-developed dorsomedial part of the human Nr consists of densely packed cells, deriving small myelinated fibers that continue into the medial central tegmental tract.Based on these findings we suggest there are distinct bipedal-quadrupedal differences for Nr projections to the olivary complex.The human NB may be distinguished from its more specialised ND (ND lies alongside a well-developed pNr) in the human central gray.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, School of Medicine, Iwate Medical University, Morioka, Japan. sonodera@iwate-med.ac.jp

ABSTRACT

Background: The human red nucleus (Nr) is comparatively less well-studied than that of cats or monkeys. Given the functional importance of reticular and midbrain structures in control of movement and locomotion as well as from an evolutionary perspective, we investigated the nature and extent of any differences in Nr projections to the olivary complex in quadrupedal and bipedal species. Using neuroanatomical tract-tracing techniques we developed a "neural sheet" hypothesis allowing us to propose how rubro-olivary relations differ among the three species.

Methods and findings: Wheat germ agglutinin-horseradish peroxidase staining supports findings that the cat's nucleus accessories medialis of Bechtrew (NB) projects mainly to the lateral bend of the principal olive. We clarified boundaries among nucleus of Darkschewitsch (ND), NB and parvicellular red nucleus (pNr) of the cat's neural sheet. The macaque's ND-medial accessory olivary projection is rostro-caudally organized and the dorsomedial and ventrolateral parts of the macaque's pNr may project to the principal olive's rostral and caudal dorsal lamella; in cat it projects as well to pNr. Myelin- and Nissl-stained sections show that a well-developed dorsomedial part of the human Nr consists of densely packed cells, deriving small myelinated fibers that continue into the medial central tegmental tract.

Conclusions: Based on these findings we suggest there are distinct bipedal-quadrupedal differences for Nr projections to the olivary complex. We propose the Nr of cats and monkeys comprise the ND, NB and pNr in a zonal sheet-like structure, retaining clear nuclear boundaries and an isolated, well-developed mNr. The human NB may be distinguished from its more specialised ND (ND lies alongside a well-developed pNr) in the human central gray. Phylogenetically, the NB may have been translocated into a roll-shaped Nr in the reticular formation, the dorsomedial portion of which might correspond to the cat's and monkey's NB.

Show MeSH
Related in: MedlinePlus