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Disynaptic pyramidal excitation in forelimb motoneurons mediated via C(3)-C(4) propriospinal neurons in the Macaca
1Department of Integrative Medical Biology, Umeå University, S-901 87 Umeå, Sweden.
Abstract:
In contrast to findings in the cat, it recently has been shown that disynaptic pyramidal EPSPs only rarely are observed in forelimb motoneurons of the macaque monkey in the intact spinal cord or after a corticospinal transection in C(5). This finding has been taken to indicate that the disynaptic pyramidal excitatory pathway via C(3)-C(4) propriospinal neurons (PNs) is weakened through phylogeny when the monosynaptic cortico-motoneuronal connection has been strengthened. We reinvestigate this issue with special focus on the possibility that the inhibitory control of the C(3)-C(4) PNs may be stronger in the macaque monkey than in the cat. The effect in forelimb motoneurons of electrical stimulation in the contralateral pyramid was investigated in anesthetized macaque monkeys (Macaca fuscata). We confirmed the low frequency of disynaptic pyramidal EPSPs in forelimb motoneurons. However, after intravenous injection of strychnine, disynaptic EPSPs could be evoked in 39 of 41 forelimb motoneurons recorded after lesion of the corticospinal fibers in C5. After a corresponding lesion in C(2), disynaptic pyramidal EPSPs were observed in 2 of 25 motoneurons. In contrast to previous reports, we conclude that C(3)-C(4) PNs can mediate disynaptic pyramidal excitation in high frequency of occurrence to forelimb motoneurons in the C(6)-C(8) segments and that this transmission is under a stronger inhibitory control than in the cat. Thus, the hypothesis that the disynaptic excitatory cortico-motoneuronal pathway via the C(3)-C(4) PNs is weakened in parallel with the strengthened monosynaptic connection through phylogeny is not supported by the present findings.
Insights
The disynaptic excitatory pathway to primate forelimb motor neurons is not weakened by evolution. Instead, stronger inhibitory control in macaque monkeys, not cats, masks this pathway.
Area of Science:
- Neuroscience
- Motor Control
- Comparative Neurology
Background:
- Previous studies suggested a weakened disynaptic pyramidal excitatory pathway in macaque monkeys compared to cats.
- This was hypothesized to be due to the strengthening of the monosynaptic cortico-motoneuronal connection through phylogeny.
Purpose of the Study:
- To investigate the disynaptic pyramidal excitatory pathway to forelimb motoneurons in macaque monkeys.
- To explore the role of inhibitory control over C(3)-C(4) propriospinal neurons (PNs) in macaque monkeys compared to cats.
Main Methods:
- Electrical stimulation of the contralateral pyramid in anesthetized macaque monkeys (Macaca fuscata).
- Recording of excitatory postsynaptic potentials (EPSPs) in forelimb motoneurons.
- Lesions of corticospinal fibers in C5 and C2.
- Intravenous administration of strychnine to block inhibitory neurotransmission.
Main Results:
- Disynaptic pyramidal EPSPs were rarely observed in intact or C5-lesioned macaque monkeys.
- After strychnine administration in C5-lesioned monkeys, disynaptic EPSPs were evoked in a high percentage (39/41) of motoneurons.
- Disynaptic EPSPs were rarely observed in C2-lesioned monkeys (2/25).
Conclusions:
- The C(3)-C(4) propriospinal neurons (PNs) can mediate disynaptic pyramidal excitation to forelimb motoneurons in macaque monkeys at high frequency.
- This transmission is under significantly stronger inhibitory control in macaque monkeys than in cats.
- The hypothesis of a phylogenetically weakened disynaptic pathway is not supported; rather, enhanced inhibition masks the pathway in primates.