Evidence that long-term hyperexcitability of the sensory neuron soma induced by nerve injury in Aplysia is adaptive.
Peripheral axotomy induces long-term hyperexcitability (LTH) of centrally located sensory neuron (SN) somata in diverse species. In mammals this LTH can promote spontaneous activity of pain-related SNs, and such activity may contribute to neuropathic pain and hyperalgesia. However, few axotomized SN somata begin to fire spontaneously in any species, and why so many SNs display soma LTH after axotomy remains a mystery. Is soma LTH a side effect of injury with pathological but no adaptive consequences, or was this response selected during evolution for particular functions? A hypothesis for one function of soma LTH in nociceptive SNs in Aplysia californica is proposed: after peripheral injury that produces partial axotomy of some SNs, compensation for sensory deficits and protective sensitization are achieved by facilitating afterdischarge near the soma, which amplifies sensory input from injured peripheral fields. Four predictions of this hypothesis were confirmed in SNs that innervate the tail. First, LTH of SN somata was induced by a relatively natural axotomizing event-a small cut across part of the tail in the absence of anesthesia. Second, soma LTH was selectively expressed in SNs having axons in cut or crushed nerves rather than nearby, uninjured nerves. Third, after several weeks soma LTH began to reverse when functional recovery of the interrupted afferent pathway was shown by reestablishment of a centrally mediated siphon reflex. Fourth, axotomized SNs developed central afterdischarge that amplified sensory discharge coming from the periphery, and the after-depolarization underlying this afterdischarge was enhanced by previous axotomy.
Gasull
Xavier
X
Department of Integrative Biology and Pharmacology, University of Texas-Houston Medical School, Houston, Texas, USA.
Liao
Xiaogang
X
Dulin
Michael F
MF
Phelps
Cynthia
C
Walters
Edgar T
ET
D000222:Adaptation, Physiological; D000704:Analysis of Variance; D000818:Animals; D001048:Aplysia; D019771:Axotomy / Q000379:methods; D004307:Dose-Response Relationship, Radiation; D004558:Electric Stimulation / Q000379:methods; D017774:Long-Term Potentiation / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology / Q000528:radiation effects; D009416:Nerve Regeneration / Q000502:physiology; D009475:Neurons, Afferent / Q000502:physiology*; D018408:Patch-Clamp Techniques / Q000379:methods; D020127:Recovery of Function; D012684:Sensory Thresholds / Q000502:physiology; D013997:Time Factors; D020196:Trauma, Nervous System / Q000473:pathology / Q000503:physiopathology*