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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

Pyramidal and rubral effects after C2 DLF transection. (A–C), intracellular recordings from a LRN neuron when applying a train of three stimuli to the contralateral pyramid. (D,E), distribution of excitatory postsynaptic potential (EPSP) latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid and NR. (F,G), intracellular from another LRN neuron showing disynaptic pyramidal IPSPs (F) but no IPSPs evoked by NR stimulation (G). In inhibitory postsynaptic potentials (IPSPs; F) is shown the cord dorsum recording of the pyramidal volleys below the intracellular traces. Recording of the volleys was made rostral to the C2 DLF transection. The two arrow heads indicate the latency measurement from the positive/negative phase of the triphasic pyramidal volley to the IPSP onset. (H), distribution of IPSP latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid.
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Figure 2: Pyramidal and rubral effects after C2 DLF transection. (A–C), intracellular recordings from a LRN neuron when applying a train of three stimuli to the contralateral pyramid. (D,E), distribution of excitatory postsynaptic potential (EPSP) latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid and NR. (F,G), intracellular from another LRN neuron showing disynaptic pyramidal IPSPs (F) but no IPSPs evoked by NR stimulation (G). In inhibitory postsynaptic potentials (IPSPs; F) is shown the cord dorsum recording of the pyramidal volleys below the intracellular traces. Recording of the volleys was made rostral to the C2 DLF transection. The two arrow heads indicate the latency measurement from the positive/negative phase of the triphasic pyramidal volley to the IPSP onset. (H), distribution of IPSP latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid.

Mentions: Figure 2 shows recordings from two LRN neurones after a C2 DLF transection. The contralateral pyramid was stimulated by a train of three volleys at different strengths (Figures 2A–C). Small monosynaptic excitatory postsynaptic potentials (EPSPs) could be evoked with a threshold below 40 μA (Figure 2A). The amplitude increased when the current stimulus intensity was raised to 80 and 200 μA (Figures 2B,C). The longer EPSP duration with 200 μA is likely due to activation slower conducting corticoreticular fibers. Monosynaptic pyramidal EPSPs were observed in 25% of the neurones. Monosynaptic rubral EPSPs after C2 DLF transection was observed in 10% of the neurones (not illustrated). Lack of disynaptic cortico- or rubral EPSPs were observed in all of the 40 cells tested. The segmental latencies are shown in Figures 2D,E. In contrast, disynaptic pyramidal inhibitory postsynaptic potentials (IPSPs) could be elicited after C2 DLF transection, but at lower frequency (7/19 neurones) compared to before the lesion (33/66 neurones). One example of pyramidal disynaptic IPSPs is shown in Figure 2F. Rubral IPSPs were lacking following C2 DLF transection (0/21 neurones) and one example is shown in Figure 2G, which is taken from the same LRN cell as in (Figure 2F). These data reveal monosynaptic excitation of LRN neurons by cortico- and rubro-reticular fibers, and disynaptic pyramidal inhibition, but not from NR.


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

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

Pyramidal and rubral effects after C2 DLF transection. (A–C), intracellular recordings from a LRN neuron when applying a train of three stimuli to the contralateral pyramid. (D,E), distribution of excitatory postsynaptic potential (EPSP) latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid and NR. (F,G), intracellular from another LRN neuron showing disynaptic pyramidal IPSPs (F) but no IPSPs evoked by NR stimulation (G). In inhibitory postsynaptic potentials (IPSPs; F) is shown the cord dorsum recording of the pyramidal volleys below the intracellular traces. Recording of the volleys was made rostral to the C2 DLF transection. The two arrow heads indicate the latency measurement from the positive/negative phase of the triphasic pyramidal volley to the IPSP onset. (H), distribution of IPSP latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 2: Pyramidal and rubral effects after C2 DLF transection. (A–C), intracellular recordings from a LRN neuron when applying a train of three stimuli to the contralateral pyramid. (D,E), distribution of excitatory postsynaptic potential (EPSP) latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid and NR. (F,G), intracellular from another LRN neuron showing disynaptic pyramidal IPSPs (F) but no IPSPs evoked by NR stimulation (G). In inhibitory postsynaptic potentials (IPSPs; F) is shown the cord dorsum recording of the pyramidal volleys below the intracellular traces. Recording of the volleys was made rostral to the C2 DLF transection. The two arrow heads indicate the latency measurement from the positive/negative phase of the triphasic pyramidal volley to the IPSP onset. (H), distribution of IPSP latencies measured from the incoming volley evoked by stimulation in the contralateral pyramid.
Mentions: Figure 2 shows recordings from two LRN neurones after a C2 DLF transection. The contralateral pyramid was stimulated by a train of three volleys at different strengths (Figures 2A–C). Small monosynaptic excitatory postsynaptic potentials (EPSPs) could be evoked with a threshold below 40 μA (Figure 2A). The amplitude increased when the current stimulus intensity was raised to 80 and 200 μA (Figures 2B,C). The longer EPSP duration with 200 μA is likely due to activation slower conducting corticoreticular fibers. Monosynaptic pyramidal EPSPs were observed in 25% of the neurones. Monosynaptic rubral EPSPs after C2 DLF transection was observed in 10% of the neurones (not illustrated). Lack of disynaptic cortico- or rubral EPSPs were observed in all of the 40 cells tested. The segmental latencies are shown in Figures 2D,E. In contrast, disynaptic pyramidal inhibitory postsynaptic potentials (IPSPs) could be elicited after C2 DLF transection, but at lower frequency (7/19 neurones) compared to before the lesion (33/66 neurones). One example of pyramidal disynaptic IPSPs is shown in Figure 2F. Rubral IPSPs were lacking following C2 DLF transection (0/21 neurones) and one example is shown in Figure 2G, which is taken from the same LRN cell as in (Figure 2F). These data reveal monosynaptic excitation of LRN neurons by cortico- and rubro-reticular fibers, and disynaptic pyramidal inhibition, but not from NR.

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