Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species

Striking differences in transmission of corticospinal excitation to upper limb motoneurons in two primate species
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DOI:
10.1152/jn.2000.84.2.698
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发表时间:
2000-08-01
影响因子:
2.5
通讯作者:
Lemon, RN
Lemon, RN
中科院分区:
医学3区
文献类型:
--
作者:
Nakajima, K;Maier, MA;Lemon, RN

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对于上肢运动的皮质控制,直接皮质运动神经元(CM)与间接的皮质脊髓兴奋到颈部运动神经元的固有脊髓传递的相对重要性存在相当大的争论。在没有CM连接的猫中,相当大比例的皮质脊髓兴奋通过C-3-C-4本体脊髓神经元(PN)系统到达前肢运动神经元。相比之下,在猕猴大多数运动神经元直接CM连接,并在相同的实验条件下,在猫,有PN传输的证据很少。我们研究了新世界松鼠猴(Saimiri sciureus)的皮质脊髓传递,因为它的CM预测比猕猴弱。细胞内记录从运动神经元确定的尺,正中,和深桡(DR)神经在四个成年松鼠猴氯醛糖麻醉和神经肌肉麻痹。在C-5背外侧索(DLF)损伤之前和之后记录对侧延髓锥体刺激的反应,旨在中断对下颈段的直接皮质脊髓输入并揭示PN介导的效应。这种损伤大大降低了运动神经元表现CM EPSP或双突触IPSP的比例,但表现出由重复而非单一PT刺激诱发的节段性延长超出单突触范围的迟发EPSP的比例不受影响:损伤前29个运动神经元中有23个(79%),损伤后37个运动神经元中有32个(86%); 41%的晚期EPSP在损伤后有严格的双突触延长,而损伤前只有14%。这些结果与猕猴形成鲜明对比(C5损伤前仅18%的运动神经元出现晚期EPSP,C5损伤后为19%)。在松鼠猴中,通过C-3-C-4 PN的晚期EPSP的传递由其在额外的C-2 DLF损伤后的缺失指示。几乎所有的测试运动神经元也响应于短潜伏期EPSP刺激同侧外侧网状核。通过与猫的类比,这些EPSP可能反映了C-3-C-4 PN与运动神经元的单突触连接的上行侧支的逆向激活; EPSP显著小于猫,但大于猕猴。这些结果表明,更先进的手功能和CM系统的强度之间的正相关性,伴随着手功能和PN系统的强度之间的负相关性。我们假设,在灵长类动物更先进的手功能,CM系统有效地取代PN介导的控制。这将包括一个贡献的控制达到运动,这是说,特别是在猫的PN系统的控制下,我们推测,这些差异可能与不同物种所表现出的灵巧程度。这种解释的结果预测,在人,CM系统是高度发达的,PN系统是不可能负责显着的传输皮层命令上肢运动神经元。
There is considerable debate as to the relative importance, for cortical control of upper limb movements, of direct cortico-motoneuronal (CM) versus indirect, propriospinal transmission of corticospinal excitation to cervical motoneurons. In the cat, which has no CM connections, a significant proportion of corticospinal excitation reaches forelimb motoneurons via a system of C-3-C-4 propriospinal neurons (PN). In contrast, in the macaque monkey most motoneurons receive direct CM connections, and, under the same experimental conditions as in the cat, there is little evidence for PN transmission. We have investigated corticospinal transmission in the New World squirrel monkey (Saimiri sciureus) because its CM projections are weaker than in the macaque. Intracellular recordings were made from motoneurons identified from the ulnar, median, and deep radial (DR) nerves in four adult squirrel monkeys under chloralose anesthesia and neuromuscular paralysis. Responses to stimulation of the contralateral medullary pyramid were recorded before and after a lesion to the dorsolateral funiculus (DLF) at C-5, designed to interrupt direct corticospinal inputs to the lower cervical segments and unmask PN-mediated effects. This lesion greatly reduced the proportion of motoneurons showing either CM EPSPs or disynaptic IPSPs, but the proportion showing late EPSPs with segmental latencies beyond the monosynaptic range, evoked by repetitive but not single PT stimuli, was unaffected: 23 of 29 motoneurons (79%) before and 32 of 37 (86%) after the lesion; 41% of these late EPSPs had strictly disynaptic latencies after the lesion, only 14% before. These results are in striking contrast to the macaque (late EPSPs in only 18% of motoneurons before a C5 lesion, 19% after it). Transmission of the late EPSPs via C-3-C-4 PNs in the squirrel monkey was indicated by their absence after an additional C-2 DLF lesion. Nearly all tested motoneurons also responded with short latency EPSPs to stimulation in the ipsilateral lateral reticular nucleus. By analogy with the cat, these EPSPs probably reflect antidromic activation of ascending collaterals of C-3-C-4 PNs with monosynaptic connections to motoneurons; the EPSPs were significantly smaller than in the cat but larger than in the macaque. These results suggest that the positive correlation across species between more advanced hand function and the strength of the CM system is accompanied by a negative correlation between hand function and the strength of the PN system. We hypothesize that in primates with more advanced hand function, the CM system effectively replaces PN-mediated control. This would include a contribution to the control of reaching movements, which are said to be specifically under the control of the PN system in the cat, and we speculate that these differences may be related to the degree of dexterity exhibited by the different species. This interpretation of the results predicts that in man, where the CM system is highly developed, the PN system is unlikely to be responsible for significant transmission of cortical commands to upper limb motoneurons.