Limitations on impulse conduction at the branch point of afferent axons in frog dorsal root ganglion

Abstract

Impulse conduction at the branch point of afferent axons in dorsal root ganglion (DRG) has been studied using intracellular recording from frog DRG neurons in vitro. The least conduction interval (LCI, the minimum inter-response interval) was determined for pairs of impulses to successfully propagate through the branch point into the dorsal root. At 21 degrees-23 degrees C, average branch point LCI was significantly longer than for afferent fibers in the peripheral nerve. This result suggested that the branch point would limit the maximum frequency of action potentials that could conduct into the dorsal root. This was found to be the case. The maximum frequency of impulses in short trains (less than or equal to 40 ms) which could conduct into the dorsal root without failure (363 Hz) was accurately predicted by branch point LCI and was far less than the maximum frequency predicted from the LCI of axons in the peripheral nerve (610 Hz). Branch point LCI was correlated (r = -0.78) with the natural log of peripheral axon conduction velocity (CV). However, the relationship of LCI and CV was different for different types of neurons and the shape of the somatic action potential was found to be a reliable predictor of branch point LCI. Neurons with long-duration somatic action potentials with a shoulder on the falling phase tended to have low CV and invariably had long LCI's. Neurons with brief, smooth action potentials had short LCI's regardless of CV. These cells, which appear to be the most differentiated type, have found a way to minimize branch point LCI which is virtually independent of their axonal CV. For the latter neurons, branch point LCI was correlated (r = 0.42) with the reciprocal of the hyperpolarization level, at the cell body, required to block conduction through the branch point, suggesting that the proximity of the cell body to the branch point might play a role in determining the LCI of some neurons. Over a range of 12 degrees C to around 35 degrees C, branch point LCI was inversely related and maximum firing frequency directly related to temperature. At high temperatures (30 degrees-40 degrees C) conduction failure occurred at sites having particularly long LCI's. It is concluded that a) these axon branch points act as low-pass filters and set the maximum frequency of conducted impulses that can access the central nervous system; b) certain varieties of DRG neurons exhibit more branch point filtering action than others; and c) warming, within limits, reduces branch point filtering action.

Two Opposing Roles of 4-AP–Sensitive K+ Current in Initiation and Invasion of Spikes in Rat Mesencephalic Trigeminal Neurons

“…Nevertheless, whenever an impulse arising from the peripheral axon failed to invade the stem axon, it also failed to invade the central axon, as demonstrated in frog DRG neurons (Stoney 1990). Taken together with the present findings on the spike initiation mechanism in the stem axon, it is likely that impulses arising from the peripheral axon trigger impulses in the stem axon before they reach the branching point, and then invade into the soma and simultaneously propagate forward through the central axon (Fig.…”

Time Course and Nerve Growth Factor Dependence of Inflammation-Induced Alterations in Electrophysiological Membrane Properties in Nociceptive Primary Afferent Neurons

“…1C). In some units (not related to f unctional properties) three sizes of potential were recorded: f ull size, approximately half size, and very small (as also reported by Stoney, 1990). The two different sizes of electrotonic response (the half-sized and small responses) appear to indicate that failure could occur at two sites.…”

Heat Stress–Mediated Plasticity in a Locust Looming-Sensitive Visual Interneuron

“…During high-frequency activity, refractory effects can threaten conduction reliability (Grossman et al 1979;Zhou and Chiu 2001). Decreased action potential amplitude and conduction failure during high-frequency spiking has been shown in both myelinated (Lüscher et al 1983;Soleng et al 2003;Stoney 1990) and unmyelinated axon (Grossman et al 1979;Smith 1980). Amplitude attenuation can result from the inactivation of voltage-gated sodium current (Rudy 1981).…”

“…Decreased amplitude and duration of action potentials at high temperature are thought to contribute to conduction failures (Lüscher et al 1983;Stoney 1990;Westerfield et al 1978). With respect to locust action potentials, increased temperature not only decreases amplitude and duration, but also hyperpolarizes membrane potentials and reduces input resistance (Abrams and Pearson 1982;Burrows 1989;Heitler et al 1977;Simmons 1990;Wu et al 2001;Xu and Robertson 1994).…”