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Historical reflections on the afterhyperpolarization–firing rate relation of vertebrate spinal neurons

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Abstract

In mammalian spinal motoneurons (MNs), the slow component of the afterhyperpolarization (AHP) that follows the spike of each action potential is a major but not the sole determinant of the cells' firing rate. In this brief historical review, we emphasize four points about the AHP-firing rate relation. (1) There is a relatively sparse literature across vertebrates that directly addresses this topic. (2) After the advent of intracellular recording in the early 1950s, there was evidence from mammals to the contrary of an idea that subsequently became prevalent: that the high-firing rates attainable by spinal interneurons (INs) and low-threshold MNs was attributable to their small AHP at rheobase. (3) Further work is needed to determine whether our present findings on the AHP-firing rate relation of turtle cells generalize to the spinal neurons of other vertebrate species. (4) Relevant to point 3, substantial in vivo and in vitro work is potentially available in raw data used in reports on several mammalian and non-mammalian vertebrates. In summary, the factors in addition to the slow AHP that help determine spinal INs and MN firing rate deserve further evaluation across vertebrates, with relevant data already potentially available in several laboratories.

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Notes

  1. In vertebrates, the fast (f) component of the AHP typically follows the K+ delayed rectifier conductance, which is largely responsible for spike repolarization. This fAHP lasts 2–10 ms and has a minimal effect on firing rate (Fig. 1 in Nordstrom et al. 2007). The subsequent slow (s) component of the AHP as discussed in this review is sometimes termed “medium (m)” (Binder et al. 1996; Powers and Binder 2001) in mammals in order to distinguish it from a very slow component, which has been shown to last several seconds in several vertebrate species, including mammals (Sah 1996). The latter include, for example: selected cells in the hippocampus, olfactory bulb, and neocortex; vagal MNs of the brainstem; and, peripheral sensory and autonomic ganglia. Such very slow AHPs have not been observed, however, in mammalian spinal MNs and INs (Powers and Binder 2001) and turtle MNs and INs (Hounsgaard and Mintz 1988; Hounsgaard et al. 1988; McDonagh et al. 1998; Hornby et al. 2002).

  2. In the adult turtle, we have shown that the evolution of the AHP in spinal INs from rheobase to maximum firing rate features a relatively smooth, continuous decrease in size as the cells transitioned from the single response to the continuously discharging response (Stauffer et al. 2005b, 2006). In contrast, spinal MNs (both low- and high-threshold) showed an increase of AHP when they converted from rheobase to minimum firing rate and then a continuous decrease up to the maximum firing rate (Stauffer et al. 2005b, 2006). At equal but relatively low firing rates (<7 Hz), AHP size was larger for low-threshold spinal MNs than for high-threshold spinal MNs. At equal firing rates ≥8 Hz, there was no difference in AHP size between the two groups of MNs (Stauffer et al. 2006) and at rates greater than ∼20 Hz, AHP size converged toward a similar value for both INs and MNs (unpublished observation). Despite the larger AHP at the lower rates, the low-threshold MNs attained much higher maximum rates (∼54 Hz) than did the high-threshold MNs (∼27 Hz) (Stauffer et al. 2005b).

  3. Spike-frequency adaptation is defined as a decline in firing rate in the presence of a sustained, constant depolarizing pressure exerted on a neuron by intracellular current injection. In adult cat spinal MNs, its initial phase occurs within the first second of repetitive discharge and is now usually attributed to some species-dependent combination of AHP summation and a slow inactivation of NaT, the fast, transient Na+ conductance. The AHP summation is thought to be brought on by increased Ca2+ entry leading to a greater activation of the Ca2+-dependent K+ channel responsible for the slow (medium in cat) AHP: i.e., primarily the KCa(Sk) conductance. The later phases of spike-frequency adaptation appear to involve some species- and context-dependent combination of (1) an increase in the decay time of GkCa(Sk), (2) increased activity of the Na+/K+ pump, (3) increased Na+ channel inactivation (both NaT and NaP, the persistent Na+ conductance), and (4) a decreased persistent inward current attributable to decreased GCa(L) and GNa(P). (for review of the above, see Powers et al. 1999; Miles et al. 2005; Zeng et al. 2005; Kernell 2006; Nordstrom et al. 2007).

  4. Such studies include: fish-pyramidal cells of lateral line lobe (Lemon and Turner 2000); zebrafish-neurons of lateral magnocellular nucleus (Livingston and Mooney 2001); mouse-neocortical neurons (Erisir et al. 1999); rat (proceeding rostrally)-dorsal vagal neurons (Lewis et al. 2002); facial MNs (Magarinos-Ascone et al. 1999); locus coerulus noradrenergic neurons (also in monkey; Horvath et al. 1999); suprachiasmatic nucleus cells (Cloues and Sather 2003); ventral pallidal cells (Bengston and Osborne 2000); hippocampal neurons (Savic et al. 2001); guinea pig-hypothalamic γ-aminobutyric acid neurons (Wagner et al. 2001); and cat-medullary respiratory neurons (Baeky et al. 2001); oculomotor neurons (Trigo et al. 1999); sensorimotor cortical neurons (Nishimura et al. 2001).

  5. Similar results have recently been obtained in dorsal horn neurons of slices of adult mouse spinal cord, using in vitro patch-clamp recording (Graham et al. 2006). Again the AHP amplitude was substantial (25–30 mV) at rheobase and low firing rates, and peak steady-state firing rates were up to 100 Hz at room temperature.

Abbreviations

AHP:

Afterhyperpolarization

AP:

Action potential

I–f:

Stimulus current−spike frequency

IN:

Interneuron

MN:

Motoneuron

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Acknowledgments

We thank Robert Brownstone and Randall Powers for reviewing a draft of this manuscript. Their viewpoints do not necessarily coincide precisely with those expressed in this report. We also thank Patricia Pierce for her technical and editorial help. The project was supported in part by: an Edwin Eddy Foundation Award (to E. K. S.); USPHS grants NS 20577 and NS 07309 (to D. G. S.), NS 20762 and NS 01686 (to J. C. M.), and GM O8400 (to W. H. Dantzler); and a Flinn Foundation Fellowship and an Award from the American Psychological Association Minority Program in Neuroscience (to T. G. H.).

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  1. T. G. Hornby

    Present address: Department of Physical Therapy, UIC, Chicago, IL, 60612, USA

  2. R. M. Reinking

    Present address: Program in Applied Mathematics, The University of Arizona, Tucson, AZ, 85721-0089, USA

Authors and Affiliations

  1. Department of Physiology and Pharmacology, The University of Minnesota, Duluth, MN, 55812-3031, USA

    E. K. Stauffer

  2. Department of Physiology, The University of Arizona, Tucson, AZ, 85724-5051, USA

    J. C. McDonagh & D. G. Stuart

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  1. E. K. Stauffer
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  2. J. C. McDonagh
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  3. T. G. Hornby
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  5. D. G. Stuart
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Correspondence to D. G. Stuart.

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Stauffer, E.K., McDonagh, J.C., Hornby, T.G. et al. Historical reflections on the afterhyperpolarization–firing rate relation of vertebrate spinal neurons. J Comp Physiol A 193, 145–158 (2007). https://doi.org/10.1007/s00359-006-0198-2

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