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The lateral reticular nucleus; integration of descending and ascending systems regulating voluntary forelimb movements.

Alstermark B, Ekerot CF - Front Comput Neurosci (2015)

Bottom Line: Individual motoneurones do not have projections to spino-cerebellar neurons.The LRN projections to the deep cerebellar nuclei exert a direct excitatory effect on descending motor pathways via the reticulospinal, vestibulospinal, and other supraspinal tracts, and might play a key role in cerebellar motor control.Our results support the hypothesis that the LRN provides the cerebellum with highly integrated information, enabling cerebellar control of complex forelimb movements.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Medical Biology, Section of Physiology, Umeå University Umeå, Sweden.

ABSTRACT
Cerebellar control of movements is dependent on mossy fiber input conveying information about sensory and premotor activity in the spinal cord. While much is known about spino-cerebellar systems, which provide the cerebellum with detailed sensory information, much less is known about systems conveying motor information. Individual motoneurones do not have projections to spino-cerebellar neurons. Instead, the fastest route is from last order spinal interneurons. In order to identify the networks that convey ascending premotor information from last order interneurons, we have focused on the lateral reticular nucleus (LRN), which provides the major mossy fiber input to cerebellum from spinal interneuronal systems. Three spinal ascending systems to the LRN have been investigated: the C3-C4 propriospinal neurones (PNs), the ipsilateral forelimb tract (iFT) and the bilateral ventral flexor reflex tract (bVFRT). Voluntary forelimb movements involve reaching and grasping together with necessary postural adjustments and each of these three interneuronal systems likely contribute to specific aspects of forelimb motor control. It has been demonstrated that the command for reaching can be mediated via C3-C4 PNs, while the command for grasping is conveyed via segmental interneurons in the forelimb segments. Our results reveal convergence of ascending projections from all three interneuronal systems in the LRN, producing distinct combinations of excitation and inhibition. We have also identified a separate descending control of LRN neurons exerted via a subgroup of cortico-reticular neurones. The LRN projections to the deep cerebellar nuclei exert a direct excitatory effect on descending motor pathways via the reticulospinal, vestibulospinal, and other supraspinal tracts, and might play a key role in cerebellar motor control. Our results support the hypothesis that the LRN provides the cerebellum with highly integrated information, enabling cerebellar control of complex forelimb movements.

No MeSH data available.


Related in: MedlinePlus

Schematic outline of the experimental set-up. Intracellular recordings were made from antidromically identified neurones in the lateral reticular nucleus (LRN) by electrical stimulation in the cerebellar (Cer) white matter. Possible convergence from bifurcating C3-C4 propriospinal neurones (C3-C4 PNs), which project to LRN neurones and motoneurones (MNs) in the forelimb segments C6-Th1; ipsilateral forelimb tract (iFT); and the bilateral flexor reflex tract (bVFRT) was tested in LRN neurones using electrical stimulation. C3-C4 PNs were activated from fibers in the contralateral pyramid (Pyr) and nucleus ruber (NR) after transection of these fibers in the dorsolateral funiculus (DLF) in C5. A control lesion was made in C2 to eliminate cortico-and rubrospinal input to C3-C4 PNs. C3-C4 PNs could also be activated by stimulation of cortico- and rubrospinal fibers in the DLF in the C3-C4 segments following DLF transections in both C5 and C2. iFT neurones were activated by stimulation of primary afferents in the ipsilateral superficial (SR) and deep radial (DR) nerves (SR and DR) after transection of the dorsal column (DC) in C5 to eliminate afferent input to the more rostrally located C3-C4 PNs. bVFRT neurones were activated from the contralateral SR and DR nerves after a DC transection in C5 and from the lateral vestibulospinal tract (LVST) via stimulation in the contralateral ventral quadrant (cVQ) in C4 or C6. In order to prevent activation of bVFRT neurones in the lumbar segments by LVST stimulation, the contralateral spinal cord was transected at Th13. The lumbar bVFRT neurons were activated by stimulation of the LVST caudal to lesion in in Th13.
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Figure 1: Schematic outline of the experimental set-up. Intracellular recordings were made from antidromically identified neurones in the lateral reticular nucleus (LRN) by electrical stimulation in the cerebellar (Cer) white matter. Possible convergence from bifurcating C3-C4 propriospinal neurones (C3-C4 PNs), which project to LRN neurones and motoneurones (MNs) in the forelimb segments C6-Th1; ipsilateral forelimb tract (iFT); and the bilateral flexor reflex tract (bVFRT) was tested in LRN neurones using electrical stimulation. C3-C4 PNs were activated from fibers in the contralateral pyramid (Pyr) and nucleus ruber (NR) after transection of these fibers in the dorsolateral funiculus (DLF) in C5. A control lesion was made in C2 to eliminate cortico-and rubrospinal input to C3-C4 PNs. C3-C4 PNs could also be activated by stimulation of cortico- and rubrospinal fibers in the DLF in the C3-C4 segments following DLF transections in both C5 and C2. iFT neurones were activated by stimulation of primary afferents in the ipsilateral superficial (SR) and deep radial (DR) nerves (SR and DR) after transection of the dorsal column (DC) in C5 to eliminate afferent input to the more rostrally located C3-C4 PNs. bVFRT neurones were activated from the contralateral SR and DR nerves after a DC transection in C5 and from the lateral vestibulospinal tract (LVST) via stimulation in the contralateral ventral quadrant (cVQ) in C4 or C6. In order to prevent activation of bVFRT neurones in the lumbar segments by LVST stimulation, the contralateral spinal cord was transected at Th13. The lumbar bVFRT neurons were activated by stimulation of the LVST caudal to lesion in in Th13.

Mentions: The experimental setup is shown in Figure 1. Corticofugal fibers were stimulated in the contralateral pyramid (Pyr) 3–4 mm rostral to obex at the caudal end of the 4th ventricle, rubrospinal fibers in the contralateral NR (NR; Horsley-Clarke coordinates A3, L1.5, H-2.5), and fibers in the lateral vestibulospinal tract (LVST) were stimulated in the contralateral ventral quadrant (coVQ) either in C4 or C6 using monopolar tungsten electrodes, and in Th13 using bipolar silver electrodes. To restrict the activation of the bVFRT to the cervical cord, the dorsal columns (DC) were removed and a hemisection contralateral to the recording side was performed in Th11. Intracellular recording was made with glass microelectrodes filled with 2 M potassium acetate (tip diameter 1.0–2.0 μm, impedance 2–5 MΩ). LRN neurones were identified via antidromic activation from the ipsilateral cerebellar white matter dorsal to the interpositus nucleus at a depth of 6 mm below the cerebellar surface (insertion point of the electrode: 1–2 mm caudal to the primary fissure at a laterality of 4 mm). The arrival of the incoming volley to the LRN neurons was recorded by silver ball electrode at the surface near the patch used for the intracellular recordings. The stimulating and recording sites were verified histologically. The position of NR was also verified by recording the antidromic response followed by stimulation of the rubrospinal axons in Th13.


The lateral reticular nucleus; integration of descending and ascending systems regulating voluntary forelimb movements.

Alstermark B, Ekerot CF - Front Comput Neurosci (2015)

Schematic outline of the experimental set-up. Intracellular recordings were made from antidromically identified neurones in the lateral reticular nucleus (LRN) by electrical stimulation in the cerebellar (Cer) white matter. Possible convergence from bifurcating C3-C4 propriospinal neurones (C3-C4 PNs), which project to LRN neurones and motoneurones (MNs) in the forelimb segments C6-Th1; ipsilateral forelimb tract (iFT); and the bilateral flexor reflex tract (bVFRT) was tested in LRN neurones using electrical stimulation. C3-C4 PNs were activated from fibers in the contralateral pyramid (Pyr) and nucleus ruber (NR) after transection of these fibers in the dorsolateral funiculus (DLF) in C5. A control lesion was made in C2 to eliminate cortico-and rubrospinal input to C3-C4 PNs. C3-C4 PNs could also be activated by stimulation of cortico- and rubrospinal fibers in the DLF in the C3-C4 segments following DLF transections in both C5 and C2. iFT neurones were activated by stimulation of primary afferents in the ipsilateral superficial (SR) and deep radial (DR) nerves (SR and DR) after transection of the dorsal column (DC) in C5 to eliminate afferent input to the more rostrally located C3-C4 PNs. bVFRT neurones were activated from the contralateral SR and DR nerves after a DC transection in C5 and from the lateral vestibulospinal tract (LVST) via stimulation in the contralateral ventral quadrant (cVQ) in C4 or C6. In order to prevent activation of bVFRT neurones in the lumbar segments by LVST stimulation, the contralateral spinal cord was transected at Th13. The lumbar bVFRT neurons were activated by stimulation of the LVST caudal to lesion in in Th13.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4525057&req=5

Figure 1: Schematic outline of the experimental set-up. Intracellular recordings were made from antidromically identified neurones in the lateral reticular nucleus (LRN) by electrical stimulation in the cerebellar (Cer) white matter. Possible convergence from bifurcating C3-C4 propriospinal neurones (C3-C4 PNs), which project to LRN neurones and motoneurones (MNs) in the forelimb segments C6-Th1; ipsilateral forelimb tract (iFT); and the bilateral flexor reflex tract (bVFRT) was tested in LRN neurones using electrical stimulation. C3-C4 PNs were activated from fibers in the contralateral pyramid (Pyr) and nucleus ruber (NR) after transection of these fibers in the dorsolateral funiculus (DLF) in C5. A control lesion was made in C2 to eliminate cortico-and rubrospinal input to C3-C4 PNs. C3-C4 PNs could also be activated by stimulation of cortico- and rubrospinal fibers in the DLF in the C3-C4 segments following DLF transections in both C5 and C2. iFT neurones were activated by stimulation of primary afferents in the ipsilateral superficial (SR) and deep radial (DR) nerves (SR and DR) after transection of the dorsal column (DC) in C5 to eliminate afferent input to the more rostrally located C3-C4 PNs. bVFRT neurones were activated from the contralateral SR and DR nerves after a DC transection in C5 and from the lateral vestibulospinal tract (LVST) via stimulation in the contralateral ventral quadrant (cVQ) in C4 or C6. In order to prevent activation of bVFRT neurones in the lumbar segments by LVST stimulation, the contralateral spinal cord was transected at Th13. The lumbar bVFRT neurons were activated by stimulation of the LVST caudal to lesion in in Th13.
Mentions: The experimental setup is shown in Figure 1. Corticofugal fibers were stimulated in the contralateral pyramid (Pyr) 3–4 mm rostral to obex at the caudal end of the 4th ventricle, rubrospinal fibers in the contralateral NR (NR; Horsley-Clarke coordinates A3, L1.5, H-2.5), and fibers in the lateral vestibulospinal tract (LVST) were stimulated in the contralateral ventral quadrant (coVQ) either in C4 or C6 using monopolar tungsten electrodes, and in Th13 using bipolar silver electrodes. To restrict the activation of the bVFRT to the cervical cord, the dorsal columns (DC) were removed and a hemisection contralateral to the recording side was performed in Th11. Intracellular recording was made with glass microelectrodes filled with 2 M potassium acetate (tip diameter 1.0–2.0 μm, impedance 2–5 MΩ). LRN neurones were identified via antidromic activation from the ipsilateral cerebellar white matter dorsal to the interpositus nucleus at a depth of 6 mm below the cerebellar surface (insertion point of the electrode: 1–2 mm caudal to the primary fissure at a laterality of 4 mm). The arrival of the incoming volley to the LRN neurons was recorded by silver ball electrode at the surface near the patch used for the intracellular recordings. The stimulating and recording sites were verified histologically. The position of NR was also verified by recording the antidromic response followed by stimulation of the rubrospinal axons in Th13.

Bottom Line: Individual motoneurones do not have projections to spino-cerebellar neurons.The LRN projections to the deep cerebellar nuclei exert a direct excitatory effect on descending motor pathways via the reticulospinal, vestibulospinal, and other supraspinal tracts, and might play a key role in cerebellar motor control.Our results support the hypothesis that the LRN provides the cerebellum with highly integrated information, enabling cerebellar control of complex forelimb movements.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Medical Biology, Section of Physiology, Umeå University Umeå, Sweden.

ABSTRACT
Cerebellar control of movements is dependent on mossy fiber input conveying information about sensory and premotor activity in the spinal cord. While much is known about spino-cerebellar systems, which provide the cerebellum with detailed sensory information, much less is known about systems conveying motor information. Individual motoneurones do not have projections to spino-cerebellar neurons. Instead, the fastest route is from last order spinal interneurons. In order to identify the networks that convey ascending premotor information from last order interneurons, we have focused on the lateral reticular nucleus (LRN), which provides the major mossy fiber input to cerebellum from spinal interneuronal systems. Three spinal ascending systems to the LRN have been investigated: the C3-C4 propriospinal neurones (PNs), the ipsilateral forelimb tract (iFT) and the bilateral ventral flexor reflex tract (bVFRT). Voluntary forelimb movements involve reaching and grasping together with necessary postural adjustments and each of these three interneuronal systems likely contribute to specific aspects of forelimb motor control. It has been demonstrated that the command for reaching can be mediated via C3-C4 PNs, while the command for grasping is conveyed via segmental interneurons in the forelimb segments. Our results reveal convergence of ascending projections from all three interneuronal systems in the LRN, producing distinct combinations of excitation and inhibition. We have also identified a separate descending control of LRN neurons exerted via a subgroup of cortico-reticular neurones. The LRN projections to the deep cerebellar nuclei exert a direct excitatory effect on descending motor pathways via the reticulospinal, vestibulospinal, and other supraspinal tracts, and might play a key role in cerebellar motor control. Our results support the hypothesis that the LRN provides the cerebellum with highly integrated information, enabling cerebellar control of complex forelimb movements.

No MeSH data available.


Related in: MedlinePlus