Experimental Brain Research

, Volume 232, Issue 6, pp 2021–2033 | Cite as

Manual stimulation of the whisker pad after hypoglossal–facial anastomosis (HFA) using a Y-tube conduit does not improve recovery of whisking function

  • Umut Ozsoy
  • Bahadir Murat Demirel
  • Arzu Hizay
  • Ozlem Ozsoy
  • Janina Ankerne
  • Srebrina Angelova
  • Levent Sarikcioglu
  • Yasar Ucar
  • Murat Turhan
  • Sarah Dunlop
  • Doychin N. Angelov
Research Article

Abstract

Facial nerve injury is a common clinical trauma involving long-term functional deficits with facial asymmetry leading to associated psychological issues and social hardship. We have recently shown that repair by hypoglossal–facial or facial–facial nerve surgical end-to-end anastomosis and suture [hypoglossal–facial anastomosis (HFA) or facial–facial anastomosis (FFA)] results in collateral axonal branching, polyinnervation of neuromuscular junctions (NMJs) and poor function. We have also shown that another HFA repair procedure using an isogenic Y-tube (HFA + Y-tube) and involving a 10-mm gap reduces collateral axonal branching, but fails to reduce polyinnervation. Furthermore, we have previously demonstrated that manual stimulation (MS) of facial muscles after FFA or HFA reduces polyinnervation of NMJs and improves functional recovery. Here, we examined whether HFA + Y-tube and MS of the vibrissal muscles reduce polyinnervation and restore function. Isogenic Y-tubes were created using abdominal aortas. The proximal hypoglossal nerve was inserted into the long arm and sutured to its wall. The distal zygomatic and buccal facial nerve branches were inserted into the two short arms and likewise sutured to their walls. Manual stimulation involved gentle stroking of the vibrissal muscles by hand mimicking normal whisker movement. We evaluated vibrissal motor performance using video-based motion analysis, degree of collateral axonal branching using double retrograde labeling and the quality of NMJ reinnervation in target musculature using immunohistochemistry. MS after HFA + Y-tube reduced neither collateral branching, nor NMJ polyinnervation. Accordingly, it did not improve recovery of function. We conclude that application of MS after hypoglossal–facial nerve repair using an isogenic Y-tube is contraindicated: it does not lead to functional recovery but, rather, worsens it.

Keywords

Motoneuron Nerve repair Facial nerve Hypoglossal nerve Functional recovery Manual stimulation 

Notes

Acknowledgments

This study was financially supported by the Scientific and Technological Research Council of Turkey (TUBITAK; Science Fellowship by the Grant Programmes Department Nr. 2214 for U.O.), the Deutsche Forschungsgemeinschaft (AN 331/2, AN 331/5), the Jean-Uhrmacher Foundation (S.A.) and Akdeniz University Research Fund.

References

  1. Aldes LD (1995) Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat. J Comp Neurol 353(1):89–108PubMedCrossRefGoogle Scholar
  2. Angelov DN, Ceynowa M, Guntinas-Lichius O, Streppel M, Grosheva M, Kiryakova SI, Skouras E, Maegele M, Irintchev A, Neiss WF, Sinis N, Alvanou A, Dunlop SA (2007) Mechanical stimulation of paralyzed vibrissal muscles following facial nerve injury in adult rat promotes full recovery of whisking. Neurobiol Dis 26(1):229–242PubMedCrossRefGoogle Scholar
  3. Baker RS, Stava MW, Nelson KR, May PJ, Huffman MD, Porter JD (1994) Aberrant reinnervation of facial musculature in a subhuman primate: a correlative analysis of eyelid kinematics, muscle synkinesis, and motoneuron localization. Neurology 44(11):2165–2173PubMedCrossRefGoogle Scholar
  4. Bascom DA, Schaitkin BM, May M, Klein S (2000) Facial nerve repair: a retrospective review. Facial Plast Surg 16(4):309–313PubMedCrossRefGoogle Scholar
  5. Berg RW, Kleinfeld D (2003) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89(1):104–117PubMedCrossRefGoogle Scholar
  6. Bermejo R, Zeigler HP (2000) “Real-time” monitoring of vibrissa contacts during rodent whisking. Somatosens Mot Res 17(4):373–377PubMedCrossRefGoogle Scholar
  7. Bermejo R, Harvey M, Gao P, Zeigler HP (1996) Conditioned whisking in the rat. Somatosens Mot Res 13(3–4):225–233PubMedCrossRefGoogle Scholar
  8. Bermejo R, Houben D, Zeigler HP (1998) Optoelectronic monitoring of individual whisker movements in rats. J Neurosci Methods 83(2):89–96PubMedCrossRefGoogle Scholar
  9. Beurskens CHG (1990) The functional rehabilitation of facial muscles and facial expression. In: Castro D (ed) Facial nerve. Proceedings of the sixth international symposium on the facial nerve, Kugler, Amsterdam pp 509–511Google Scholar
  10. Bhathia S, Karmarkar S, Calabrese V (1995) Intratemporal hemangiomas involving the facial nerve: diagnosis and management. Skull Base Surg 5:227–232CrossRefGoogle Scholar
  11. Blinzinger K, Kreutzberg G (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z Zellforsch Mikrosk Anat 85(2):145–157PubMedCrossRefGoogle Scholar
  12. Brown MC, Holland RL, Hopkins WG, Keynes RJ (1981) An assessment of the spread of the signal for terminal sprouting within and between muscles. Brain Res 210(1–2):145–151PubMedCrossRefGoogle Scholar
  13. Brushart TM (1987) Neurotropism and neurotrophism. J Hand Surg Am 12(5 Pt 1):808–809PubMedCrossRefGoogle Scholar
  14. Brushart TM (1988) Preferential reinnervation of motor nerves by regenerating motor axons. J Neurosci 8(3):1026–1031PubMedGoogle Scholar
  15. Büngner O (1891) Ueber die degenerations- und regenerationsvorgänge am nerven nach verletzungen. Beitr Pathol Anat Allg Pathol 10:21–393Google Scholar
  16. Cao J, Xiao Z, Jin W, Chen B, Meng D, Ding W, Han S, Hou X, Zhu T, Yuan B, Wang J, Liang W, Dai J (2013) Induction of rat facial nerve regeneration by functional collagen scaffolds. Biomaterials 34(4):1302–1310PubMedCrossRefGoogle Scholar
  17. Carvell GE, Simons DJ (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10(8):2638–2648PubMedGoogle Scholar
  18. Caudle KL, Brown EH, Shum-Siu A, Burke DA, Magnuson TS, Voor MJ, Magnuson DS (2011) Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat. Neurorehabil Neural Repair 25(8):729–739PubMedCrossRefGoogle Scholar
  19. Coulson SE (2005) Physiotherapy rehabilitation following facial nerve paresis. In: Beurskens CHG, van Gelder RS, Heymans PG, Manni JJ, Nicolai JPA (eds) The facial palsies, complementary approaches. Lemma, Utrecht, pp 263–274Google Scholar
  20. Dohm S, Streppel M, Guntinas-Lichius O, Pesheva P, Probstmeier R, Walther M, Neiss WF, Stennert E, Angelov DN (2000) Local application of extracellular matrix proteins fails to reduce the number of axonal branches after varying reconstructive surgery on rat facial nerve. Restor Neurol Neurosci 16(2):117–126PubMedGoogle Scholar
  21. Dorfl J (1982) The musculature of the mystacial vibrissae of the white mouse. J Anat 135(Pt 1):147–154PubMedCentralPubMedGoogle Scholar
  22. Dorfl J (1985) The innervation of the mystacial region of the white mouse: a topographical study. J Anat 142:173–184PubMedCentralPubMedGoogle Scholar
  23. Fansa H, Keilhoff G, Plogmeier K, Frerichs O, Wolf G, Schneider W (1999) Successful implantation of Schwann cells in acellular muscles. J Reconstr Microsurg 15(1):61–65PubMedCrossRefGoogle Scholar
  24. Fansa H, Keilhoff G, Wolf G, Schneider W, Gold BG (2001) Tissue engineering of peripheral nerves: a comparison of venous and acellular muscle grafts with cultured schwann cells. Plast Reconstr Surg 107(2):495–496PubMedCrossRefGoogle Scholar
  25. Fansa H, Schneider W, Wolf G, Keilhoff G (2002) Influence of insulin-like growth factor-I (IGF-I) on nerve autografts and tissue-engineered nerve grafts. Muscle Nerve 26(1):87–93PubMedCrossRefGoogle Scholar
  26. Gordon T, Hegedus J, Tam SL (2004) Adaptive and maladaptive motor axonal sprouting in aging and motoneuron disease. Neurol Res 26(2):174–185PubMedCrossRefGoogle Scholar
  27. Grimby G, Einarsson G, Hedberg M, Aniansson A (1989) Muscle adaptive changes in post-polio subjects. Scand J Rehabil Med 21(1):19–26PubMedGoogle Scholar
  28. Grosheva M, Guntinas-Lichius O, Arnhold S, Skouras E, Kuerten S, Streppel M, Angelova SK, Wewetzer K, Radtke C, Dunlop SA, Angelov DN (2008) Bone marrow-derived mesenchymal stem cell transplantation does not improve quality of muscle reinnervation or recovery of motor function after facial nerve transection in rats. Biol Chem 389(7):873–888PubMedCrossRefGoogle Scholar
  29. Gundersen HJ (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143(Pt1):3–45PubMedCrossRefGoogle Scholar
  30. Guntinas-Lichius O (2004) The facial nerve in the presence of a head and neck neoplasm: assessment and outcome after surgical management. Curr Opin Otolaryngol Head Neck Surg 12(2):133–141PubMedCrossRefGoogle Scholar
  31. Guntinas-Lichius O, Mockenhaupt J, Stennert E, Neiss WF (1993) Simplified nerve cell counting in the rat brainstem with the physical disector using a drawing-microscope. J Microsc 172(Pt 2):177–180PubMedCrossRefGoogle Scholar
  32. Guntinas-Lichius O, Neiss WF, Schulte E, Stennert E (1996) Quantitative image analysis of the chromatolysis in rat facial and hypoglossal motoneurons following axotomy with and without reinnervation. Cell Tissue Res 286(3):537–541PubMedCrossRefGoogle Scholar
  33. Guntinas-Lichius O, Angelov DN, Tomov TL, Dramiga J, Neiss WF, Wewetzer K (2001) Transplantation of olfactory ensheathing cells stimulates the collateral sprouting from axotomized adult rat facial motoneurons. Exp Neurol 172(1):70–80PubMedCrossRefGoogle Scholar
  34. Guntinas-Lichius O, Wewetzer K, Tomov TL, Azzolin N, Kazemi S, Streppel M, Neiss WF, Angelov DN (2002) Transplantation of olfactory mucosa minimizes axonal branching and promotes the recovery of vibrissae motor performance after facial nerve repair in rats. J Neurosci 22(16):7121–7131PubMedGoogle Scholar
  35. Guntinas-Lichius O, Irintchev A, Streppel M, Lenzen M, Grosheva M, Wewetzer K, Neiss WF, Angelov DN (2005) Factors limiting motor recovery after facial nerve transection in the rat: combined structural and functional analyses. Eur J Neurosci 21(2):391–402PubMedCrossRefGoogle Scholar
  36. Guntinas-Lichius O, Hundeshagen G, Paling T, Streppel M, Grosheva M, Irintchev A, Skouras E, Alvanou A, Angelova SK, Kuerten S, Sinis N, Dunlop SA, Angelov DN (2007) Manual stimulation of facial muscles improves functional recovery after hypoglossal–facial anastomosis and interpositional nerve grafting of the facial nerve in adult rats. Neurobiol Dis 28(1):101–112PubMedCrossRefGoogle Scholar
  37. Haastert K, Grosheva M, Angelova SK, Guntinas-Lichius O, Skouras E, Michael J, Grothe C, Dunlop SA, Angelov DN (2009) Schwann cells overexpressing FGF-2 alone or combined with manual stimulation do not promote functional recovery after facial nerve injury. J Biomed Biotechnol 2009:408794PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hadlock T, Kowaleski J, Mackinnon S, Heaton JT (2007) A novel method of head fixation for the study of rodent facial function. Exp Neurol 205(1):279–282PubMedCentralPubMedCrossRefGoogle Scholar
  39. Hadlock T, Lindsay R, Edwards C, Smitson C, Weinberg J, Knox C, Heaton JT (2010) The effect of electrical and mechanical stimulation on the regenerating rodent facial nerve. Laryngoscope 120(6):1094–1102PubMedGoogle Scholar
  40. Hizay A, Ozsoy U, Demirel BM, Ozsoy O, Angelova SK, Ankerne J, Sarikcioglu SB, Dunlop SA, Angelov DN, Sarikcioglu L (2012) Use of a Y-tube conduit after facial nerve injury reduces collateral axonal branching at the lesion site but neither reduces polyinnervation of motor endplates nor improves functional recovery. Neurosurgery 70(6):1544–1556PubMedCrossRefGoogle Scholar
  41. Hudson TW, Evans GR, Schmidt CE (2000) Engineering strategies for peripheral nerve repair. Orthop Clin North Am 31(3):485–498PubMedCrossRefGoogle Scholar
  42. IJpma FF, Nicolai JP, Meek MF (2006) Sural nerve donor-site morbidity: thirty-four years of follow-up. Ann Plast Surg 57(4):391–395PubMedCrossRefGoogle Scholar
  43. Inada Y, Hosoi H, Yamashita A, Morimoto S, Tatsumi H, Notazawa S, Kanemaru S, Nakamura T (2007) Regeneration of peripheral motor nerve gaps with a polyglycolic acid-collagen tube: technical case report. Neurosurgery 61(5):E1105–E1107PubMedCrossRefGoogle Scholar
  44. Ito M, Kudo M (1994) Reinnervation by axon collaterals from single facial motoneurons to multiple muscle targets following axotomy in the adult guinea pig. Acta Anat (Basel) 151(2):124–130CrossRefGoogle Scholar
  45. Johnson EO, Soucacos PN (2008) Nerve repair: experimental and clinical evaluation of biodegradable artificial nerve guides. Injury 39(Suppl 3):S30–S36PubMedCrossRefGoogle Scholar
  46. Kerrebijn JD, Freeman JL (1998) Facial nerve reconstruction: outcome and failures. J Otolaryngol 27(4):183–186PubMedGoogle Scholar
  47. Komisaruk BR (1970) Synchrony between limbic system theta activity and rhythmical behavior in rats. J Comp Physiol Psychol 70(3):482–492PubMedCrossRefGoogle Scholar
  48. Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: a HRP study in the rat. Brain Res 170(3):533–537PubMedCrossRefGoogle Scholar
  49. Kunihiro T, Higashino K, Kanzaki J (2003) Classic hypoglossal–facial nerve anastomosis after acoustic neuroma resection. A review of 46 cases. ORL J Otorhinolaryngol Relat Spec 65(1):1–6PubMedCrossRefGoogle Scholar
  50. Lundborg G, Dahlin LB, Danielsen N, Nachemson AK (1986) Tissue specificity in nerve regeneration. Scand J Plast Reconstr Surg 20(3):279–283PubMedCrossRefGoogle Scholar
  51. Lundborg G, Rosen B, Dahlin L, Danielsen N, Holmberg J (1997) Tubular versus conventional repair of median and ulnar nerves in the human forearm: early results from a prospective, randomized, clinical study. J Hand Surg Am 22(1):99–106PubMedCrossRefGoogle Scholar
  52. Mackinnon SE, Dellon AL (1988) A comparison of nerve regeneration across a sural nerve graft and a vascularized pseudosheath. J Hand Surg Am 13(6):935–942PubMedCrossRefGoogle Scholar
  53. Manni JJ, Beurskens CH, van de Velde C, Stokroos RJ (2001) Reanimation of the paralyzed face by indirect hypoglossal–facial nerve anastomosis. Am J Surg 182(3):268–273PubMedCrossRefGoogle Scholar
  54. Martins RS, Teodoro WR, Simplicio H, Capellozi VL, Siqueira MG, Yoshinari NH, Pereira JP, Teixeira MJ (2011) Influence of suture on peripheral nerve regeneration and collagen production at the site of neurorrhaphy: an experimental study. Neurosurgery 68(3):765–772PubMedCrossRefGoogle Scholar
  55. May M (1986) Surgical rehabilitation of facial palsy. In: May M (ed) The facial nerve. Thieme, New York, pp 695–777Google Scholar
  56. Midha R, Munro CA, Dalton PD, Tator CH, Shoichet MS (2003) Growth factor enhancement of peripheral nerve regeneration through a novel synthetic hydrogel tube. J Neurosurg 99(3):555–565PubMedCrossRefGoogle Scholar
  57. Millesi H (1981) Interfascicular nerve grafting. Orthop Clin North Am 12(2):287–301PubMedGoogle Scholar
  58. Morin D, Monteau R, Hilaire G (1992) Compared effects of serotonin on cervical and hypoglossal inspiratory activities: an in vitro study in the newborn rat. J Physiol 451:605–629PubMedCentralPubMedGoogle Scholar
  59. Morris JH, Hudson AR, Weddell G (1972) A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy. I. The traumatic degeneration of myelin in the proximal stump of the divided nerve. Z Zellforsch Mikrosk Anat 124(1):76–102PubMedCrossRefGoogle Scholar
  60. Naff NJ, Ecklund JM (2001) History of peripheral nerve surgery techniques. Neurosurg Clin N Am 12(1):197–209PubMedGoogle Scholar
  61. Neiss WF, Guntinas Lichius O, Angelov DN, Gunkel A, Stennert E (1992) The hypoglossal–facial anastomosis as model of neuronal plasticity in the rat. Ann Anat 174(5):419–433PubMedCrossRefGoogle Scholar
  62. Ozsoy U, Demirel BM, Hizay A, Ozsoy O, Ankerne J, Angelova S, Sarikcioglu L, Ucar Y, Angelov DN (2011) Hypoglossal–facial anastomosis (HFA) over a 10 mm gap bridged by a Y-tube-conduit enhances neurite regrowth and reduces collateral axonal branching at the lesion site. Restor Neurol Neurosci 29(4):227–242PubMedGoogle Scholar
  63. Pavlov SP, Grosheva M, Streppel M, Guntinas-Lichius O, Irintchev A, Skouras E, Angelova SK, Kuerten S, Sinis N, Dunlop SA, Angelov DN (2008) Manually-stimulated recovery of motor function after facial nerve injury requires intact sensory input. Exp Neurol 211(1):292–300PubMedCrossRefGoogle Scholar
  64. Pinganaud G, Bernat I, Buisseret P, Buisseret-Delmas C (1999) Trigeminal projections to hypoglossal and facial motor nuclei in the rat. J Comp Neurol 415(1):91–104PubMedCrossRefGoogle Scholar
  65. Politis MJ (1985) Specificity in mammalian peripheral nerve regeneration at the level of the nerve trunk. Brain Res 328(2):271–276PubMedCrossRefGoogle Scholar
  66. Politis MJ, Ederle K, Spencer PS (1982) Tropism in nerve regeneration in vivo. Attraction of regenerating axons by diffusible factors derived from cells in distal nerve stumps of transected peripheral nerves. Brain Res 253(1–2):1–12PubMedCrossRefGoogle Scholar
  67. Prokopenko AV, Shum-Siu A, Wainwright GN, Seibt E, Magnuson DSK (2013) Muscle stretch reduces locomotor function after a spinal cord injury: acute and chronic time points. Paper presented at the 15th international symposium on neural regeneration, Asilomar, California, 11–15 Dec 2013Google Scholar
  68. Quist BW, Hartmann MJ (2008) A two-dimensional force sensor in the millinewton range for measuring vibrissal contacts. J Neurosci Methods 172(2):158–167PubMedCrossRefGoogle Scholar
  69. Rich MM, Lichtman JW (1989) In vivo visualization of pre- and postsynaptic changes during synapse elimination in reinnervated mouse muscle. J Neurosci 9(5):1781–1805PubMedGoogle Scholar
  70. Saleh E, Achilli V, Naguib M, Taibah AK, Russo A, Sanna M, Mazzoni A (1995) Facial nerve neuromas: diagnosis and management. Am J Otol 16(4):521–526PubMedGoogle Scholar
  71. Schultz JD, Dodson TB, Meyer RA (1992) Donor site morbidity of greater auricular nerve graft harvesting. J Oral Maxillofac Surg 50(8):803–805PubMedCrossRefGoogle Scholar
  72. Seckel BR, Ryan SE, Gagne RG, Chiu TH, Watkins E Jr (1986) Target-specific nerve regeneration through a nerve guide in the rat. Plast Reconstr Surg 78(6):793–800PubMedCrossRefGoogle Scholar
  73. Semba K, Egger MD (1986) The facial “motor” nerve of the rat: control of vibrissal movement and examination of motor and sensory components. J Comp Neurol 247(2):144–158PubMedCrossRefGoogle Scholar
  74. Semba K, Komisaruk BR (1984) Neural substrates of two different rhythmical vibrissal movements in the rat. Neuroscience 12(3):761–774PubMedCrossRefGoogle Scholar
  75. Semba K, Szechtman H, Komisaruk BR (1980) Synchrony among rhythmical facial tremor, neocortical ‘alpha’ waves, and thalamic non-sensory neuronal bursts in intact awake rats. Brain Res 195(2):281–298PubMedCrossRefGoogle Scholar
  76. Shawe GD (1955) On the number of branches formed by regenerating nerve-fibres. Br J Surg 42(175):474–488PubMedCrossRefGoogle Scholar
  77. Son YJ, Trachtenberg JT, Thompson WJ (1996) Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions. Trends Neurosci 19(7):280–285PubMedCrossRefGoogle Scholar
  78. Stennert E, Limberg C (1982) Central connections between fifth, seventh, and twelfth cranial nerves and their clinical significance. In: Graham MDHW (ed) Disorders of the facial nerve. Raven, New York, pp 57–65Google Scholar
  79. Streppel M, Azzolin N, Dohm S, Guntinas-Lichius O, Haas C, Grothe C, Wevers A, Neiss WF, Angelov DN (2002) Focal application of neutralizing antibodies to soluble neurotrophic factors reduces collateral axonal branching after peripheral nerve lesion. Eur J Neurosci 15(8):1327–1342PubMedCrossRefGoogle Scholar
  80. Suarez V, Guntinas-Lichius O, Streppel M, Ingorokva S, Grosheva M, Neiss WF, Angelov DN, Klimaschewski L (2006) The axotomy-induced neuropeptides galanin and pituitary adenylate cyclase-activating peptide promote axonal sprouting of primary afferent and cranial motor neurones. Eur J Neurosci 24(6):1555–1564PubMedCrossRefGoogle Scholar
  81. Tam SL, Archibald V, Jassar B, Tyreman N, Gordon T (2001) Increased neuromuscular activity reduces sprouting in partially denervated muscles. J Neurosci 21(2):654–667PubMedGoogle Scholar
  82. Tankere F, Bernat I, Vitte E, Lamas G, Soudant J, Maisonobe T, Bouche P, Fournier E, Willer JC (2004) The hypolossal-facial anastomosis in man. A model for studying peripheral and central nervous system plasticity. Rev Med Liege 59(Suppl 1):91–103PubMedGoogle Scholar
  83. Tomov TL, Guntinas-Lichius O, Grosheva M, Streppel M, Schraermeyer U, Neiss WF, Angelov DN (2002) An example of neural plasticity evoked by putative behavioral demand and early use of vibrissal hairs after facial nerve transection. Exp Neurol 178(2):207–218PubMedCrossRefGoogle Scholar
  84. Tos P, Battiston B, Geuna S, Giacobini-Robecchi MG, Hill MA, Lanzetta M, Owen ER (2000) Tissue specificity in rat peripheral nerve regeneration through combined skeletal muscle and vein conduit grafts. Microsurgery 20(2):65–71PubMedCrossRefGoogle Scholar
  85. Towal RB, Hartmann MJ (2008) Variability in velocity profiles during free-air whisking behavior of unrestrained rats. J Neurophysiol 100(2):740–752PubMedCrossRefGoogle Scholar
  86. Trojan DA, Gendron D, Cashman NR (1991) Electrophysiology and electrodiagnosis of the post-polio motor unit. Orthopedics 14(12):1353–1361PubMedGoogle Scholar
  87. Uemura-Sumi M, Itoh M, Mizuno N (1988) The distribution of hypoglossal motoneurons in the dog, rabbit and rat. Anat Embryol (Berl) 177(5):389–394CrossRefGoogle Scholar
  88. Vleggeert-Lankamp CL, de Ruiter GC, Wolfs JF, Pego AP, Feirabend HK, Lakke EA, Malessy MJ (2005) Type grouping in skeletal muscles after experimental reinnervation: another explanation. Eur J Neurosci 21(5):1249–1256PubMedCrossRefGoogle Scholar
  89. Williams LR (1987) Rat aorta isografts possess nerve regeneration-promoting properties in silicone Y chambers. Exp Neurol 97(3):555–563PubMedCrossRefGoogle Scholar
  90. Zerari-Mailly F, Pinganaud G, Dauvergne C, Buisseret P, Buisseret-Delmas C (2001) Trigemino-reticulo-facial and trigemino-reticulo-hypoglossal pathways in the rat. J Comp Neurol 429(1):80–93PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Umut Ozsoy
    • 1
  • Bahadir Murat Demirel
    • 1
  • Arzu Hizay
    • 1
  • Ozlem Ozsoy
    • 2
  • Janina Ankerne
    • 3
  • Srebrina Angelova
    • 4
  • Levent Sarikcioglu
    • 1
  • Yasar Ucar
    • 1
  • Murat Turhan
    • 5
  • Sarah Dunlop
    • 6
  • Doychin N. Angelov
    • 3
  1. 1.Department of Anatomy, Faculty of MedicineAkdeniz UniversityAntalyaTurkey
  2. 2.Department of Physiology, Faculty of MedicineAkdeniz UniversityAntalyaTurkey
  3. 3.Anatomical Institute IUniversity of CologneCologneGermany
  4. 4.Department of Oto-Rhino-LaryngologyUniversity of CologneCologneGermany
  5. 5.Department of Oto-Rhino-Laryngology, Faculty of MedicineAkdeniz UniversityAntalyaTurkey
  6. 6.School of Animal BiologyThe University of Western AustraliaCrawleyAustralia

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