Are all spinal segments equal: intrinsic membrane properties of superficial dorsal horn neurons in the developing and mature mouse spinal cord

Authors

  • M. A. Tadros,

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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  • B. M. Harris,

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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  • W. B. Anderson,

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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  • A. M. Brichta,

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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  • B. A. Graham,

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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  • R. J. Callister

    1. School of Biomedical Sciences and Pharmacy, Faculty of Health and Hunter Medical Research Institute, University of Newcastle, Callaghan, NSW 2308, Australia
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R. J. Callister: School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, NSW 2308, Australia. Email: robert.callister@newcastle.edu.au

Abstract

Key points 

  • • Much of what we know about pain signalling in the spinal cord comes from studies undertaken in lumbosacral spinal segments that innervate the hindlimb.
  • • Clinical evidence suggests sensory information from viscera and head and neck tissues is processed differently from sensations arising in the hindlimb.
  • • Here we show that intrinsic membrane properties, a major determinate of neuronal output, change dramatically during development in superficial dorsal horn (SDH) neurons from lumbar, thoracic and upper cervical segments in the mouse. In contrast, intrinsic membrane properties are generally conserved in SDH neurons along the length of the spinal cord in both neonates and adults.
  • • Our data suggest the intrinsic membrane properties of SDH neurons involved in pain signalling do not contribute to the marked differences in pain experienced in the limbs, viscera and head and neck.

Abstract

Abstract  Neurons in the superficial dorsal horn (SDH; laminae I–II) of the spinal cord process nociceptive information from skin, muscle, joints and viscera. Most of what we know about the intrinsic properties of SDH neurons comes from studies in lumbar segments of the cord even though clinical evidence suggests nociceptive signals from viscera and head and neck tissues are processed differently. This ‘lumbar-centric’ view of spinal pain processing mechanisms also applies to developing SDH neurons. Here we ask whether the intrinsic membrane properties of SDH neurons differ across spinal cord segments in both the developing and mature spinal cord. Whole cell recordings were made from SDH neurons in slices of upper cervical (C2–4), thoracic (T8–10) and lumbar (L3–5) segments in neonatal (P0–5) and adult (P24–45) mice. Neuronal input resistance (RIN), resting membrane potential, AP amplitude, half-width and AHP amplitude were similar across spinal cord regions in both neonates and adults (∼100 neurons for each region and age). In contrast, these intrinsic membrane properties differed dramatically between neonates and adults. Five types of AP discharge were observed during depolarizing current injection. In neonates, single spiking dominated (∼40%) and the proportions of each discharge category did not differ across spinal regions. In adults, initial bursting dominated in each spinal region, but was significantly more prevalent in rostral segments (49% of neurons in C2–4 vs. 29% in L3–5). During development the dominant AP discharge pattern changed from single spiking to initial bursting. The rapid A-type potassium current (IAr) dominated in neonates and adults, but its prevalence decreased (∼80%vs. ∼50% of neurons) in all regions during development. IAr steady state inactivation and activation also changed in upper cervical and lumbar regions during development. Together, our data show the intrinsic properties of SDH neurons are generally conserved in the three spinal cord regions examined in both neonate and adult mice. We propose the conserved intrinsic membrane properties of SDH neurons along the length of the spinal cord cannot explain the marked differences in pain experienced in the limbs, viscera, and head and neck.

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