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Properties of Propriospinal Neurons in the C₃–C₄ Segments Mediating Disynaptic Pyramidal Excitation to Forelimb Motoneurons in the Macaque Monkey

¹Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Japan; ²Department of Physiology, Kyorin University Medical School, Tokyo, Japan; ³Department of Integrative Medical Biology, Section of Physiology, Umeå University, Umeå, Sweden; and ⁴Core Research for Evolutionary Science and Technology of Japan Science and Technology Agency, Kawaguchi, Japan

Submitted 28 January 2005; accepted in final form 29 January 2006

Candidate propriospinal neurons (PNs) that mediate disynaptic pyramidal excitation to forelimb motoneurons were studied in the C₃–C₄ segments in anesthetized macaque monkeys (n = 10). A total of 177 neurons were recorded (145 extracellularly, 48 intracellularly, and 16 both) in laminae VI–VII. Among these, 86 neurons (73 extracellularly, 14 intracellularly and 1 both) were antidromically activated from the forelimb motor nucleus or from the ventrolateral funiculus just lateral to the motor nucleus in the C₆/C₇ segments and thus are identified as PNs. Among the 73 extracellularly recorded PNs, 60 cells were fired by a train of four stimuli to the contralateral pyramid with segmental latencies of 0.8–2.2 ms, with most of them (n = 52) in a monosynaptic range (<1.4 ms including one synaptic delay and time to firing). The firing probability was only 21% from the third pyramidal volley but increased to 83% after intravenous injection of strychnine. In most of the intracellularly recorded PNs, stimulation of the contralateral pyramid evoked monosynaptic excitatory postsynaptic potentials (EPSPs, 12/14) and disynaptic inhibitory postsynaptic potentials (14/14), which were found to be glycinergic. In contrast, cells that did not project to the C₆–Th₁ segments where forelimb motoneurons are located were classified as segmental interneurons. These were fired from the third pyramidal volley with a probability of 71% before injection of strychnine. It is proposed that some of these interneurons mediate feed-forward inhibition to the PNs. These results suggest that the C₃–C₄ PNs receive feed-forward inhibition from the pyramid in addition to monosynaptic excitation and that this inhibition is stronger in the macaque monkey than in the cat. Another difference with the cat was that only 26 of the 86 PNs (30%, as compared with 84% in the cat) with projection to the forelimb motor nuclei send ascending collaterals terminating in the lateral reticular nucleus (LRN) on the ipsilateral side of the medulla. Thus we identified C₃–C₄ PNs that could mediate disynaptic pyramidal excitation to forelimb motoneurons in the macaque monkey. The present findings explain why it was difficult in previous studies of the macaque monkey to evoke disynaptic pyramidal excitation via C₃–C₄ PNs in forelimb motoneurons and why—as compared with the cat—the monosynaptic EPSPs evoked from the LRN via C₃–C₄ PNs were smaller in amplitude.

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