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Afterhyperpolarization–firing rate relation of turtle spinal neurons

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Abstract

This study addressed the afterhyperploarization–firing rate relationship of unanesthetized turtle spinal motoneurons and interneurons. The afterhyperploarization of their solitary action potential at rheobase was compared to that during the cells’ minimum and maximum firing rates. Like previous mammalian findings, afterhyperpolarization duration and area at rheobase were 32 and 19% less for high- versus low-threshold motoneurons. Contrariwise, maximum firing rate was two times less for the high-threshold group. Other new findings were that for high- versus low-threshold interneurons, afterhyperpolarization duration and area were 25 and 95% less, and maximum firing rate 21% higher for the high-threshold group. For combined motoneurons versus interneurons, there were no differences in afterhyperpolarization duration and area at rheobase, whereas maximum firing rate was 265% higher for the interneurons. For high-threshold motoneurons alone, there were significant associations between minimum firing rate and afterhyperpolarization duration and area measured at rheobase. In summary, this study showed that (1) the afterhyperploarization values of both turtle spinal motoneurons and interneurons at rheobase provided little indication of their corresponding values at the cells’ minimum and maximum firing states, and (2) the evolution of afterhyperploarization from rheobase to maximum firing state differed both qualitatively and quantitatively for motoneurons versus interneurons.

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Abbreviations

AHP :

Afterhyperpolarization

AP :

Action potential

f/I slope:

Slope of the I–f relation

f max :

Peak AP spike-frequency of I–f relation

f min :

Spike frequency at Imin

ht :

High threshold

I-f relation:

Stimulus current–spike frequency relation

I max :

Stimulus current at fmax

I min :

Threshold stimulus current for repetitive AP discharge

IN :

Interneuron

lt :

Low threshold

MN :

Motoneuron

ISI :

Interspike interval

References

  • Baldissera F, Gustafsson B (1971) Regulation of repetitive firing in motoneurones by afterhyperpolarization conductance. Brain Res 30:431–443

    Article  CAS  PubMed  Google Scholar 

  • Baldissera F, Gustafsson B (1974) Firing behaviour of a neurone model based on afterhyperpolarization conductance time course and algebraical summation. Adaptation and steady state firing. Acta Physiol Scand 92:27–47

    CAS  PubMed  Google Scholar 

  • Baldissera F, Gustafsson B, Parmiggiani F (1976) A model for refractoriness accumulation and secondary range firing in spinal motoneurones. Biol Cybern 24:61–65

    Article  Google Scholar 

  • Binder MD (2002) Integration of synaptic and intrinsic dendritic currents in cat spinal motoneurons. Brain Res Rev 40:1–8

    Google Scholar 

  • Binder MD, Heckman CJ, Powers RK (1996) The physiological control of motoneuron activity. In: Rowell LB, Shepherd JT (eds) Handbook of physiology, sect 12. Exercise: regulation and integration of multiple systems. Oxford University Press, New York, pp 3–53

    Google Scholar 

  • Breitwieser GE (1996) Mechanisms of K+ channel regulation. J Membr Biol 152:1–11

    Google Scholar 

  • Brownstone RM, Jordan LM, Kriellaars DJ, Noga B, Shefchyk SJ (1992) On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res 90:441–455

    Article  CAS  PubMed  Google Scholar 

  • Buchanan JT (1993) Electrophysiological properties of identified classes of lamprey spinal neurons. J Neurophysiol 70:2313–2325

    CAS  PubMed  Google Scholar 

  • Callister RJ, Laidlaw DH, Stuart DG (1995) A commentary on the segmental motor system of the turtle: implications for the study of its cellular mechanisms and interactions. J Morphol 225:213–227

    CAS  PubMed  Google Scholar 

  • Callister RJ, Peterson EH, Brichta AM (1999) Neuromuscular strategies underlying ballistic movements. Prog Brain Res 123:233–243

    CAS  PubMed  Google Scholar 

  • Eccles JC, Eccles RM, Lundberg A (1958) The action potentials of the alpha motoneurones supplying fast and slow muscles. J Physiol (Lond) 142:275–291

    CAS  Google Scholar 

  • Gorman RB, Reinking RM, Stuart DG (1995) Characterization of the biophysical properties of spinal neurons: a solution using a graphical programming language. Sci Tech J 5:22–25

    Google Scholar 

  • Graham BA, Brichta AM, Callister RJ (2004) In vivo responses of mouse superficial dorsal horn neurones to both current injecton and peripheral cutaneous stimulation. J Physiol (Lond) Oct 7: Epub ahead of print

  • Gritti I, Manns ID, Mainville L, Jones BE (2003) Paravalumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458:11–31

    Article  PubMed  Google Scholar 

  • Guertin PA, Hounsgaard J (1999) Non-volatile general anesthetics reduce spinal activity by suppressing plateau potentials. Neuroscience 88:353–358

    Article  CAS  PubMed  Google Scholar 

  • Haapanen L, Kolmodin GM, Skoglund CR (1958) Membrane and action potentials of spinal interneurons in the cat. Acta Physiol Scand 43:315–348

    CAS  PubMed  Google Scholar 

  • Hashiguchi-Ikeda M, Namba T, Ishii TM, Hisano T, Fukuda K (2003) Halothane inhibits an intermediate conductance Ca2+-activated K+ channel by acting at the extracellular side of the ionic pore. Anesthesiology 99:1340–1345

    Article  CAS  PubMed  Google Scholar 

  • Hille B (2001) Ion channels of excitable membranes. Sinauer, Sunderland, pp 143–147

    Google Scholar 

  • Hornby TG, McDonagh JC, Reinking RM, Stuart DG (2002a) Motoneurons: a preferred firing range across vertebrate species? Muscle Nerve 25:632–648

    Article  PubMed  Google Scholar 

  • Hornby TG, McDonagh JC, Reinking, RM, Stuart DG (2002b) Electrophysiological properties of spinal motoneurons in the adult turtle. J Comp Physiol A 188:397–408

    Article  CAS  Google Scholar 

  • Hounsgaard J, Kjærulff O (1992) Ca2+-mediated plateau potentials in a subpopulation of interneurons in the ventral horn of the turtle spinal cord. Eur J Neurosci 4:183–188

    PubMed  Google Scholar 

  • Hounsgaard J, Mintz I (1988) Calcium conductance and firing properties of spinal motoneurones in the turtle. J Physiol (Lond) 398:591–603

    CAS  Google Scholar 

  • Hounsgaard J, Kiehn O, Mintz I (1988a) Response properties of motoneurons in a slice preparation of the turtle spinal cord. J Physiol (Lond) 398:575–589

    CAS  Google Scholar 

  • Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1988b) Bistability of α-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol (Lond) 405:345–367

    CAS  Google Scholar 

  • Ito M, Oshima T (1962) Temporal summation of after hyperpolarization following a motoneuron spike. Nature 195:910–911

    Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Oxford University Press, New York, pp 317–323

    Google Scholar 

  • Jankowska E (2001) Organisation of inputs to spinal interneurone populations. J Physiol (Lond) 533:31–40

    Article  CAS  Google Scholar 

  • Kernell D (1965a) The adaptation and the relation between discharge frequency and current strength of cat lumbosacral motoneurones stimulated by long-lasting injected currents. Acta Physiol Scand 65:65–73

    Google Scholar 

  • Kernell D (1965b) High-frequency repetitive firing of cat lumbosacral motoneurones stimulated by long-lasting injected currents. Acta Physiol Scand 65:74–86

    Google Scholar 

  • Kernell D (1965c) The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 65:87–100

    Google Scholar 

  • Kernell D (1979) Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat. Brain Res 160:159–162

    Article  CAS  PubMed  Google Scholar 

  • Kernell D (1983) Functional properties of spinal motoneurones and the gradation of muscle force. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven Press, New York, pp 213–226

    Google Scholar 

  • Kernell D (1990) Spinal motoneurons and their muscle fibers: mechanisms and long-term consequences of common activation patterns. In: Binder MD, Mendell LM (eds) The segmental motor system. Oxford University Press, New York, pp 36–57

    Google Scholar 

  • Kernell D (1992) Organized variability in the neuromuscular system: a survey of task-related adaptations. Arch Ital Biol 130:19–66

    CAS  PubMed  Google Scholar 

  • Kernell D (1999) Repetitive impulse firing in motoneurons: facts and perspectives. Prog Brain Res 123:31–37

    CAS  PubMed  Google Scholar 

  • Kernell D (2002) Things we know and do not know about motoneurones. Adv Exp Biol Med 508:187–192

    Google Scholar 

  • Kernell D, Sjoholm H (1972) Motoneurone models based on ‘voltage clamp equations’ for peripheral nerve. Acta Physiol Scand 86:546–562

    CAS  PubMed  Google Scholar 

  • Kernell D, Sjoholm H (1973) Repetitive impulse firing: comparisons between neurone models based on ‘voltage clamp equations’ and spinal motoneurones. Acta Physiol Scand 87:40–56

    CAS  PubMed  Google Scholar 

  • Kernell D, Bakels R, Copray JC (1999) Discharge properties of motoneurones: how are they matched to the properties and use of their muscle units? J Physiol (Paris) 93:87–96

    Article  CAS  Google Scholar 

  • Kiehn O, Butt SJ (2003) Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70:357–361

    Article  Google Scholar 

  • Martin G, Puig S, Pietrzykowski A, Zadek P, Emery P, Treistman S (2004) Somatic localization of a specific large-conductance calcium-activated potassium channel subtype controls compartmentalized ethanol sensitivity in the nucleus accumbens. J Neurosci 24:6563–6572

    Article  CAS  PubMed  Google Scholar 

  • Matthews PBC (1996) Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol (Lond) 492:597–628

    CAS  Google Scholar 

  • McDonagh JC, Gorman RB, Gilliam EE, Hornby TG, Reinking RM, Stuart DG (1998) Properties of spinal motoneurones and interneurons in the adult turtle: provisional classification by cluster analysis. J Comp Neurol 400:544–570

    Article  CAS  PubMed  Google Scholar 

  • McDonagh JC, Callister RJ, Brichta AM, Reinking RM, Stuart DG (1999a) A commentary on the properties of spinal interneurons versus motoneurons in vertebrates, and their firing-rate behavior during movement. In: Gantchev G (ed) Motor control today and tomorrow. Academic Publishing House “Prof. M. Drinov”, Sofia, pp 3–29

    Google Scholar 

  • McDonagh JC, Gorman RB, Gilliam EE, Hornby TG, Reinking RM, Stuart DG (1999b) Electrophysiological and morphological properties of neurons in the ventral horn of the turtle spinal cord. J Physiol (Paris) 93:3–16

    Article  CAS  Google Scholar 

  • McDonagh JC, Hornby TG, Reinking RM, Stuart DG (2002) Associations between the morphology and physiology of ventral-horn neurons in the adult turtle. J Comp Neurol 454:177–191

    Article  PubMed  Google Scholar 

  • Megias M, Alvarez-Otero R, Pombal MA (2003) Calbindin and calretinin immunoreactivities identify different types of neurons in the adult lamprey spinal cord. J Comp Neurol 455:72–85

    Article  CAS  PubMed  Google Scholar 

  • Powers RK (1993) A variable-threshold motoneuron model that incorporates time- and voltage-dependent potassium and calcium conductances. J Neurophysiol 70:246–262

    CAS  PubMed  Google Scholar 

  • Powers RK, Binder MD (2000) Relationship between the time course of the afterhyperpolarization and discharge variability in cat spinal motoneurones. J Physiol (Lond) 528:131–150

    Article  CAS  Google Scholar 

  • Powers RK, Binder MD (2001) Input–output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143:137–263

    CAS  PubMed  Google Scholar 

  • Powers RK, Sawczuk A, Musick JR, Binder MD (1999) Multiple mechanisms of spike-frequency adaptation in motoneurones. J Physiol (Paris) 93:101–114

    Article  CAS  Google Scholar 

  • Prescott SA, De Koninck Y (2002) Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. J Physiol (Lond) 539:817–836

    Article  CAS  Google Scholar 

  • Sah P (1996) Ca2+-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci 19:150–154

    Article  CAS  PubMed  Google Scholar 

  • Sah P, Davies P (2000) Calcium-activated potassium currents in mammalian neurons. Clin Exp Pharm Physiol 27:657–663

    Article  CAS  Google Scholar 

  • Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66:345–353

    Article  CAS  PubMed  Google Scholar 

  • Saunders PA, Ho IK (1990) Barbiturates and the GABAA receptor complex. Prog Drug Res 34:261–268

    CAS  PubMed  Google Scholar 

  • Sawczuk A, Powers RK, Binder MD (1995) Spike frequency adaptation studied in hypoglossal motoneurons of the rat. J Neurophysiol 73:1799–1810

    CAS  PubMed  Google Scholar 

  • Sawczuk A, Powers RK, Binder MD (1997) Contribution of outward currents to spike-frequency adaptation in hypoglossal motoneurons of the rat. J Neurophysiol 78:2246–2253

    CAS  PubMed  Google Scholar 

  • Schwaller B, Meyer M, Schiffmann S (2002) ‘New’ functions for ‘old’ proteins: the role of calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241–258

    Article  CAS  PubMed  Google Scholar 

  • Stauffer EK, McDonagh JM, Hornby TJ, Reinking RM, Stuart DG (2001) Does AHP predict a spinal neurons’ peak firing rate? Soc Neurosci Abstr 27:1456

    Google Scholar 

  • Villalobos C, Shakkottai VG, Chandy KG, Michelhaugh SK, Andrade R (2004) SKCa channels mediate the medium but not the slow calcium-activated afterhyperpolarization in cortical neurons. J Neurosci 24:3537–3542

    Article  CAS  PubMed  Google Scholar 

  • Yamakura T, Bertaccini E, Trudell JR, Harris RA (2001) Anesthetics and ion channels: molecular models and sites of action. Annu Rev Pharmacol Toxicol 41:23–51

    Article  CAS  PubMed  Google Scholar 

  • Zengel JE, Reid SA, Sypert GW, Munson JB (1985) Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. J Neurophysiol 53:1323–1344

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Alan Brichta, Robert Callister, Brett Graham, Daniel Kernell and Pankaj Sah for reviewing earlier drafts of this manuscript. Their viewpoints do not necessarily coincide 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.). E.K.S. thanks David Mohrman for helpful discussions. All protocols involved in the experiments that provided the database for this report were approved by the Institutional Animal Care and Use Committee of the University of Arizona and conformed with local, state, and federal regulations for the care and use of laboratory animals.

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Author notes

  1. J. C. McDonagh

    Present address: Program in Physical Therapy, Arizona School of Health Sciences, Mesa, AZ, 85206, USA

  2. T. G. Hornby

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

  3. R. M. Reinking

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

Authors and Affiliations

  1. Department of Physiology, University of Minnesota, Duluth, MN, 55812-2487, USA

    E. K. Stauffer

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

    D. G. Stuart

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

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Stauffer, E.K., Stuart, D.G., McDonagh, J.C. et al. Afterhyperpolarization–firing rate relation of turtle spinal neurons. J Comp Physiol A 191, 135–146 (2005). https://doi.org/10.1007/s00359-004-0583-7

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