Axon diameters and conduction velocities in the macaque pyramidal tract

Abstract

Small axons far outnumber larger fibers in the corticospinal tract, but the function of these small axons remains poorly understood. This is because they are difficult to identify, and therefore their physiology remains obscure. To assess the extent of the mismatch between anatomic and physiological measures, we compared conduction time and velocity in a large number of macaque corticospinal neurons with the distribution of axon diameters at the level of the medullary pyramid, using both light and electron microscopy. At the electron microscopic level, a total of 4,172 axons were sampled from 2 adult male macaque monkeys. We confirmed that there were virtually no unmyelinated fibers in the pyramidal tract. About 14% of pyramidal tract axons had a diameter smaller than 0.50 μm (including myelin sheath), most of these remaining undetected using light microscopy, and 52% were smaller than 1 μm. In the electrophysiological study, we determined the distribution of antidromic latencies of pyramidal tract neurons, recorded in primary motor cortex, ventral premotor cortex, and supplementary motor area and identified by pyramidal tract stimulation (799 pyramidal tract neurons, 7 adult awake macaques) or orthodromically from corticospinal axons recorded at the mid-cervical spinal level (192 axons, 5 adult anesthetized macaques). The distribution of antidromic and orthodromic latencies of corticospinal neurons was strongly biased toward those with large, fast-conducting axons. Axons smaller than 3 μm and with a conduction velocity below 18 m/s were grossly underrepresented in our electrophysiological recordings, and those below 1 μm (6 m/s) were probably not represented at all. The identity, location, and function of the majority of corticospinal neurons with small, slowly conducting axons remains unknown.

Comparative morphology of gigantopyramidal neurons in primary motor cortex across mammals

“…Many panthers hunt by stalking and pouncing on prey, which demands a substantial burst of energy, considerable strength, and the quick recruitment/coordination of many muscle groups. In modulating downstream neuromuscular output, gigantopyramidal neurons in the motor cortex exhibit several functional characteristics that may make them particularly important for feliforms: (1) they appear to be able to synchronize their activity because of dendritic bundling (Meyer, ; Scheibel et al, ) and clustering (Groos, Ewing, Carter, & Coulter, ), particularly in the hand‐forepaw region (Rivara et al ); (2) they exhibit increased conduction velocities because of their large axonal diameter (Evarts, ; Firmin et al, ; Sakai & Woody, ), and are associated, at least indirectly, with increased striated muscle contraction velocity and power (Buller, Eccles, & Eccles, ; Kohn & Noakes, ; Salmons & Vrbová, ); and finally, (3) they appear to initiate incipient, patterned downstream motor activity quickly (Lundberg & Voorhoeve, ; Takahashi, ). These functional characteristics of gigantopyramidal neurons seem consistent with, if not a prerequisite for, the unusually short reaction times in feliforms (Kohn et al ; Kohn & Noakes, ).…”

Expression of Kv3.1b potassium channel is widespread in macaque motor cortex pyramidal cells: A histological comparison between rat and macaque

“…However, Vigneswaran et al () also reported spike durations of “unidentified” neurons in M1 (those not responding antidromically to PT stimulation). Because of size bias in cortical recordings (see Firmin et al, ), these spikes are unlikely to have come from interneurons. Instead, these “unidentified neurons” were more likely to be other large M1 pyramidal cells projecting to different subcortical structures (corticostriatal, corticorubral, corticobulbar, and so forth), but not to the spinal cord.…”

Quantifying axonal responses in patient-specific models of subthalamic deep brain stimulation

“…The vast majority of axons in the CNS have fiber diameters below 4 µm [Liewald et al, 2014; Aboitiz et al, 1992], except pyramidal axons whose diameters, although predominantly between 2 µm and 4 µm, can range up to 12 µm [Firmin et al, 2014]. Nonetheless, it is the largest diameter axons that dominate the response to electrical stimulation due to their low stimulation thresholds [McNeal, 1976].…”