Cerebral Cortex, Vol. 12, No. 3, 281-296,
March 2002
© 2002 Oxford University Press
Differences in the Corticospinal Projection from Primary Motor Cortex and Supplementary Motor Area to Macaque Upper Limb Motoneurons: An Anatomical and Electrophysiological Study
Sobell Department of Neurophysiology, Institute of Neurology, University College London, London, UK, , 1 INSERM U. 483, Université Pierre et Marie Curie, 75005 Paris, France, , 2 CNRS & Université de la Mediterranée, Faculté des Sciences du Sport, Marseille, France and , 3 Department of Life Sciences, Chung Shan Medical and Dental College, Taichung 402, Taiwan
Address correspondence to Professor Roger Lemon, Sobell Department of Neurophysiology, Institute of Neurology, University College London, Queen Square, London WC1N 3BG, UK. Email rlemon{at}ion.ucl.ac.uk.
To further our understanding of the functional roles of different motor cortical areas, we made a quantitative comparison of the density of corticospinal projections from primary motor cortex (M1) and supplementary motor area (SMA) to spinal motor nuclei supplying hand and finger muscles in four macaque monkeys. We also compared the action of corticospinal outputs excited by electrical stimulation of these two areas on upper limb motoneurons recorded in three anaesthetized macaques. The hand representations of SMA and M1 were first identified using structural magnetic resonance imaging scans and intracortical microstimulation. In the anatomical study we then made focal injections of wheatgerm agglutinin– horseradish peroxidase into these representations, which were subsequently confirmed by analysis of retrograde cortical labelling. Densitometric analysis showed that corticospinal projections from M1 were denser and occupied a greater proportion of the hand muscle motor nuclei than did projections from SMA. In caudal Th1 the densest projections from M1 occupied 81% of this motoneuronal area, compared with only 6% from SMA. In the electrophysiological study, bipolar intracortical stimulation of the hand representation of M1 and SMA evoked direct (D) and indirect (I) corticospinal volleys. Volleys elicited by M1 stimulation had larger amplitudes and faster conduction velocities than those evoked from the SMA. Intracellular recordings were made from 84 contralateral upper limb motoneurons. M1 and SMA stimulation evoked markedly different responses in tested motoneurons: EPSPs were larger and more common from M1 (88% of motoneurons) than from SMA (48%). Some motoneurons (16/84) showed evidence of excitatory postsynaptic potentials mediated by monosynaptic action of the D-wave evoked from M1; these early effects were not observed from the SMA. In most motoneurons (74/84) EPSPs had segmental latencies indicating that they were due to monosynaptic action of the I-wave. The results are consistent with cortico-motoneuronal (CM) connections originating from both SMA and M1 converging upon single motoneurons, but those from M1 are far more numerous and exert stronger excitatory effects than from the SMA. Thus although they may function in parallel, the two CM projections probably make different contributions to upper limb motor control.
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