Abstract

Anatomical studies report a large proportion of fine myelinated fibers in the primate pyramidal tract (PT), while very few PT neurons (PTNs) with slow conduction velocities (CV) (<~10 m/s) are reported electrophysiologically. This discrepancy might reflect recording bias toward fast PTNs or prevention of antidromic invasion by recurrent inhibition (RI) of slow PTNs from faster axons. We investigated these factors in recordings made with a polyprobe (32 closely-spaced contacts) from motor cortex of anesthetized rats (n = 2) and macaques (n = 3), concentrating our search on PTNs with long antidromic latencies (ADLs). We identified 21 rat PTNs with ADLs >2.6 ms and estimated CV 3–8 m/s, and 67 macaque PTNs (>3.9 ms, CV 6–12 m/s). Spikes of most slow PTNs were small and present on only some recording contacts, while spikes from simultaneously recorded fast-conducting PTNs were large and appeared on all contacts. Antidromic thresholds were similar for fast and slow PTNS, while spike duration was considerably longer in slow PTNs. Most slow PTNs showed no signs of failure to respond antidromically. A number of tests, including intracortical microinjection of bicuculline (GABAA antagonist), failed to provide any evidence that RI prevented antidromic invasion of slow PTNs. Our results suggest that recording bias is the main reason why previous studies were dominated by fast PTNs.

Highlights

  • The corticospinal tract is known to subserve a number of different functions (Kuypers 1981; Lemon 2008) and this is probably reflected in the wide range of fiber diameters present in the tract, in primates (Häggqvist 1937; Lassek 1941; Firmin et al 2014)

  • While anatomical studies have emphasized the huge preponderance of fine, myelinated axons within the tract, with axon diameters of 0.5–3 μm (Häggqvist 1937; Russell and Demyer 1961; Innocenti et al 2019), recordings of antidromic responses evoked in PT neurons (PTNs) by stimulation of the pyramidal tract (PT) are dominated by responses of neurons with relatively short antidromic latencies (ADLs), indicating large, fast-conducting axons (e.g., Humphrey and Corrie 1978; Firmin et al 2014)

  • We have demonstrated that it is possible to record from slow PTNs in M1 of both macaque and rat using a multiple contact silicon probe

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Summary

Introduction

The corticospinal tract is known to subserve a number of different functions (Kuypers 1981; Lemon 2008) and this is probably reflected in the wide range of fiber diameters present in the tract, in primates (Häggqvist 1937; Lassek 1941; Firmin et al 2014). Pyramidal tract neurons (PTNs) can be antidromically activated from the PT, and studying the activity of these neurons during a wide range of motor and other tasks has been a fruitful approach to understanding corticospinal function (Evarts 1965; Turner and Delong 2000; Kraskov et al 2009; Vigneswaran et al 2011; Quallo et al 2012). Recordings from primary motor cortex (M1), premotor, and supplementary motor cortex (Evarts 1965; Humphrey and Corrie 1978; Macpherson et al 1982; Firmin et al 2014) all reveal a strong bias toward fast-conducting PTNs. Responses from ‘slow PTNs,’ with conduction velocities (CV)

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