Skip to main content
main-content
Erschienen in: Brain Structure and Function 1/2018

12.07.2017 | Original Article

Changes in the axon terminals of primary afferents from a single vibrissa in the rat trigeminal nuclei after active touch deprivation or exposure to an enriched environment

verfasst von: Julia Fernández-Montoya, Yasmina B. Martin, Pilar Negredo, Carlos Avendaño

Erschienen in: Brain Structure and Function | Ausgabe 1/2018

Einloggen, um Zugang zu erhalten

Abstract

Lasting modifications of sensory input induce structural and functional changes in the brain, but the involvement of primary sensory neurons in this plasticity has been practically ignored. Here, we examine qualitatively and quantitatively the central axonal terminations of a population of trigeminal ganglion neurons, whose peripheral axons innervate a single mystacial vibrissa. Vibrissa follicles are heavily innervated by myelinated and unmyelinated fibers that exit the follicle mainly through a single deep vibrissal nerve. We made intraneural injections of a mixture of cholera-toxin B (CTB) and isolectin B4, tracers for myelinated and unmyelinated fibers, respectively, in three groups of young adult rats: controls, animals subjected to chronic haptic touch deprivation by unilateral whisker trimming, and rats exposed for 2 months to environmental enrichment. The regional and laminar pattern of terminal arborizations in the trigeminal nuclei of the brain stem did not show gross changes after sensory input modification. However, there were significant and widespread increases in the number and size of CTB-labeled varicosities in the enriched condition, and a prominent expansion in both parameters in laminae III–IV of the caudal division of the spinal nucleus in the whisker trimming condition. No obvious changes were detected in IB4-labeled terminals in laminae I–II. These results show that a prolonged exposure to changes in sensory input without any neural damage is capable of inducing structural changes in terminals of primary afferents in mature animals, and highlight the importance of peripheral structures as the presumed earliest players in sensory experience-dependent plasticity.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Aldskogius H, Arvidsson J, Grant G (1985) The reaction of primary sensory neurons to peripheral nerve injury with particular emphasis on transganglionic changes. Brain Res Rev 10:27–46 CrossRef Aldskogius H, Arvidsson J, Grant G (1985) The reaction of primary sensory neurons to peripheral nerve injury with particular emphasis on transganglionic changes. Brain Res Rev 10:27–46 CrossRef
Zurück zum Zitat Ambalavanar R, Morris R (1993) An ultrastructural study of the binding of an alpha- d-galactose specific lectin from Griffonia simplicifolia to trigeminal ganglion neurons and the trigeminal nucleus caudalis in the rat. Neuroscience 52:699–709 CrossRefPubMed Ambalavanar R, Morris R (1993) An ultrastructural study of the binding of an alpha- d-galactose specific lectin from Griffonia simplicifolia to trigeminal ganglion neurons and the trigeminal nucleus caudalis in the rat. Neuroscience 52:699–709 CrossRefPubMed
Zurück zum Zitat Anderson RL, Gibbins IL, Morris JL (1996) Non-noradrenergic sympathetic neurons project to extramuscular feed arteries and proximal intramuscular arteries of skeletal muscles in guinea-pig hindlimbs. J Auton Nerv Syst 61:51–60 CrossRefPubMed Anderson RL, Gibbins IL, Morris JL (1996) Non-noradrenergic sympathetic neurons project to extramuscular feed arteries and proximal intramuscular arteries of skeletal muscles in guinea-pig hindlimbs. J Auton Nerv Syst 61:51–60 CrossRefPubMed
Zurück zum Zitat Arvidsson J (1982) Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 211:84–92 CrossRefPubMed Arvidsson J (1982) Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 211:84–92 CrossRefPubMed
Zurück zum Zitat Arvidsson J, Johansson K (1988) Changes in the central projection pattern of vibrissae innervating primary sensory neurons after peripheral nerve injury in the rat. Neurosci Lett 84:120–124 CrossRefPubMed Arvidsson J, Johansson K (1988) Changes in the central projection pattern of vibrissae innervating primary sensory neurons after peripheral nerve injury in the rat. Neurosci Lett 84:120–124 CrossRefPubMed
Zurück zum Zitat Arvidsson J, Rice FL (1991) Central projections of primary sensory neurons innervating different parts of the vibrissae follicles and intervibrissal skin on the mystacial pad of the rat. J Comp Neurol 309:1–16 CrossRefPubMed Arvidsson J, Rice FL (1991) Central projections of primary sensory neurons innervating different parts of the vibrissae follicles and intervibrissal skin on the mystacial pad of the rat. J Comp Neurol 309:1–16 CrossRefPubMed
Zurück zum Zitat Avendaño C (2006) Stereology of neural connections. An overview. In: Záborszky L et al (eds) Neuroanatomical tract tracing: molecules, neurons, & systems, 3rd edn. Springer, New York, pp 477–529 CrossRef Avendaño C (2006) Stereology of neural connections. An overview. In: Záborszky L et al (eds) Neuroanatomical tract tracing: molecules, neurons, & systems, 3rd edn. Springer, New York, pp 477–529 CrossRef
Zurück zum Zitat Bao L, Wang HF, Cai HJ, Tong YG, Jin SX, Lu YJ, Grant G, Hokfelt T, Zhang X (2002) Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci 16:175–185 CrossRefPubMed Bao L, Wang HF, Cai HJ, Tong YG, Jin SX, Lu YJ, Grant G, Hokfelt T, Zhang X (2002) Peripheral axotomy induces only very limited sprouting of coarse myelinated afferents into inner lamina II of rat spinal cord. Eur J Neurosci 16:175–185 CrossRefPubMed
Zurück zum Zitat Bjelke K, Aldskogius H, Arvidsson J (1996) Short- and long-term transganglionic changes in the central terminations of transected vibrissal afferents in the rat. Exp Brain Res 112:268–276 CrossRefPubMed Bjelke K, Aldskogius H, Arvidsson J (1996) Short- and long-term transganglionic changes in the central terminations of transected vibrissal afferents in the rat. Exp Brain Res 112:268–276 CrossRefPubMed
Zurück zum Zitat Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568–5572 CrossRefPubMedPubMedCentral Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568–5572 CrossRefPubMedPubMedCentral
Zurück zum Zitat Brown AG (1981) Organization in the spinal cord. The anatomy and physiology of identified neurones. Springer, Berlin Brown AG (1981) Organization in the spinal cord. The anatomy and physiology of identified neurones. Springer, Berlin
Zurück zum Zitat Cheetham CE, Barnes SJ, Albieri G, Knott GW, Finnerty GT (2012) Pansynaptic enlargement at adult cortical connections strengthened by experience. Cereb Cortex 24:521–531 CrossRefPubMedPubMedCentral Cheetham CE, Barnes SJ, Albieri G, Knott GW, Finnerty GT (2012) Pansynaptic enlargement at adult cortical connections strengthened by experience. Cereb Cortex 24:521–531 CrossRefPubMedPubMedCentral
Zurück zum Zitat Clarkson C, Antunes FM, Rubio ME (2016) Conductive hearing loss has long-lasting structural and molecular effects on presynaptic and postsynaptic structures of auditory nerve synapses in the cochlear nucleus. J Neurosci 36:10214–10227 CrossRefPubMedPubMedCentral Clarkson C, Antunes FM, Rubio ME (2016) Conductive hearing loss has long-lasting structural and molecular effects on presynaptic and postsynaptic structures of auditory nerve synapses in the cochlear nucleus. J Neurosci 36:10214–10227 CrossRefPubMedPubMedCentral
Zurück zum Zitat Coggeshall RE, Lekan HA, Doubell TP, Allchorne A, Woolf CJ (1997) Central changes in primary afferent fibers following peripheral nerve lesions. Neuroscience 77:1115–1122 CrossRefPubMed Coggeshall RE, Lekan HA, Doubell TP, Allchorne A, Woolf CJ (1997) Central changes in primary afferent fibers following peripheral nerve lesions. Neuroscience 77:1115–1122 CrossRefPubMed
Zurück zum Zitat Crissman RS, Warden RJ, Siciliano DA, Klein BG, Renehan WE, Jacquin MF, Rhoades RW (1991) Numbers of axons innervating mystacial vibrissa follicles in newborn and adult rats. Somatosens Motor Res 8:103–109 CrossRef Crissman RS, Warden RJ, Siciliano DA, Klein BG, Renehan WE, Jacquin MF, Rhoades RW (1991) Numbers of axons innervating mystacial vibrissa follicles in newborn and adult rats. Somatosens Motor Res 8:103–109 CrossRef
Zurück zum Zitat Cruz-Orive LM (1999) Precision of Cavalieri sections and slices with local errors. J Microsc 193:182–198 CrossRefPubMed Cruz-Orive LM (1999) Precision of Cavalieri sections and slices with local errors. J Microsc 193:182–198 CrossRefPubMed
Zurück zum Zitat Devonshire IM, Dommett EJ, Grandy TH, Halliday AC, Greenfield SA (2010) Environmental enrichment differentially modifies specific components of sensory-evoked activity in rat barrel cortex as revealed by simultaneous electrophysiological recordings and optical imaging in vivo. Neuroscience 170:662–669 CrossRefPubMed Devonshire IM, Dommett EJ, Grandy TH, Halliday AC, Greenfield SA (2010) Environmental enrichment differentially modifies specific components of sensory-evoked activity in rat barrel cortex as revealed by simultaneous electrophysiological recordings and optical imaging in vivo. Neuroscience 170:662–669 CrossRefPubMed
Zurück zum Zitat Diamond MC (1988) Enriching heredity. The impact of the environment on the anatomy of the brain. The Free Press, London Diamond MC (1988) Enriching heredity. The impact of the environment on the anatomy of the brain. The Free Press, London
Zurück zum Zitat Dolan S, Cahusac PM (2007) Enhanced short-latency responses in the ventral posterior medial (VPM) thalamic nucleus following whisker trimming in the adult rat. Physiol Behav 92:500–506 CrossRefPubMed Dolan S, Cahusac PM (2007) Enhanced short-latency responses in the ventral posterior medial (VPM) thalamic nucleus following whisker trimming in the adult rat. Physiol Behav 92:500–506 CrossRefPubMed
Zurück zum Zitat Ebner FF (2005) Neural plasticity in adult somatic sensory-motor systems. Taylor & Francis/CRC Press, Boca Raton CrossRef Ebner FF (2005) Neural plasticity in adult somatic sensory-motor systems. Taylor & Francis/CRC Press, Boca Raton CrossRef
Zurück zum Zitat Federmeier KD, Kleim JA, Greenough WT (2002) Learning-induced multiple synapse formation in rat cerebellar cortex. Neurosci Lett 332:180–184 CrossRefPubMed Federmeier KD, Kleim JA, Greenough WT (2002) Learning-induced multiple synapse formation in rat cerebellar cortex. Neurosci Lett 332:180–184 CrossRefPubMed
Zurück zum Zitat Fernández-Montoya J, Buendia I, Martin YB, Egea J, Negredo P, Avendano C (2016) Sensory Input-Dependent Changes in Glutamatergic Neurotransmission- Related Genes and Proteins in the Adult Rat Trigeminal Ganglion. Front Mol Neurosci 9:132 (eCollection@2016:132) CrossRefPubMedPubMedCentral Fernández-Montoya J, Buendia I, Martin YB, Egea J, Negredo P, Avendano C (2016) Sensory Input-Dependent Changes in Glutamatergic Neurotransmission- Related Genes and Proteins in the Adult Rat Trigeminal Ganglion. Front Mol Neurosci 9:132 (eCollection@2016:132) CrossRefPubMedPubMedCentral
Zurück zum Zitat Florence SL, Kaas JH (1995) Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J Neurosci 15:8083–8095 PubMed Florence SL, Kaas JH (1995) Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J Neurosci 15:8083–8095 PubMed
Zurück zum Zitat Fox K, Wong RO (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48:465–477 CrossRefPubMed Fox K, Wong RO (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48:465–477 CrossRefPubMed
Zurück zum Zitat Frostig RD (2006) Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr Opin Neurobiol 16:445–450 CrossRefPubMed Frostig RD (2006) Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr Opin Neurobiol 16:445–450 CrossRefPubMed
Zurück zum Zitat Fuchs JL, Salazar E (1998) Effects of whisker trimming on GABAA receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol 395:209–216 CrossRefPubMed Fuchs JL, Salazar E (1998) Effects of whisker trimming on GABAA receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol 395:209–216 CrossRefPubMed
Zurück zum Zitat Gogolla N, Galimberti I, Caroni P (2007) Structural plasticity of axon terminals in the adult. Curr Opin Neurobiol 17:516–524 CrossRefPubMed Gogolla N, Galimberti I, Caroni P (2007) Structural plasticity of axon terminals in the adult. Curr Opin Neurobiol 17:516–524 CrossRefPubMed
Zurück zum Zitat Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379–394 CrossRefPubMed Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sørensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379–394 CrossRefPubMed
Zurück zum Zitat Hayashi H (1980) Distributions of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase. Brain Res 183:442–446 CrossRefPubMed Hayashi H (1980) Distributions of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase. Brain Res 183:442–446 CrossRefPubMed
Zurück zum Zitat Hayashi H (1982) Differential terminal distribution of single large cutaneous afferent fibers in the spinal trigeminal nucleus and in the cervical spinal dorsal horn. Brain Res 244:173–177 CrossRefPubMed Hayashi H (1982) Differential terminal distribution of single large cutaneous afferent fibers in the spinal trigeminal nucleus and in the cervical spinal dorsal horn. Brain Res 244:173–177 CrossRefPubMed
Zurück zum Zitat Hayashi H (1985) Morphology of central terminations of intra-axonally stained, large, myelinated primary afferent fibers from facial skin in the rat. J Comp Neurol 237:195–215 CrossRefPubMed Hayashi H (1985) Morphology of central terminations of intra-axonally stained, large, myelinated primary afferent fibers from facial skin in the rat. J Comp Neurol 237:195–215 CrossRefPubMed
Zurück zum Zitat Hebb DO (1949) The organization of behavior. A neuropsychological theory. Wiley, New York Hebb DO (1949) The organization of behavior. A neuropsychological theory. Wiley, New York
Zurück zum Zitat Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647–658 CrossRefPubMed Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647–658 CrossRefPubMed
Zurück zum Zitat Huopaniemi T, Jyvasjarvi E, Carlson S, Lindroos F, Pertovaara A (1992) Response characteristics of tooth pulp-driven postsynaptic neurons in the spinal trigeminal subnucleus oralis of the cat. Acta Physiol Scand 144:177–183 CrossRefPubMed Huopaniemi T, Jyvasjarvi E, Carlson S, Lindroos F, Pertovaara A (1992) Response characteristics of tooth pulp-driven postsynaptic neurons in the spinal trigeminal subnucleus oralis of the cat. Acta Physiol Scand 144:177–183 CrossRefPubMed
Zurück zum Zitat Jacquin MF, Rhoades RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Motor Res 7:265–288 CrossRef Jacquin MF, Rhoades RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Motor Res 7:265–288 CrossRef
Zurück zum Zitat Jacquin MF, Mooney RD, Rhoades RW (1984) Axon arbors of functionally distinct whisker afferents are similar in medullary dorsal horn. Brain Res 298:175–180 CrossRefPubMed Jacquin MF, Mooney RD, Rhoades RW (1984) Axon arbors of functionally distinct whisker afferents are similar in medullary dorsal horn. Brain Res 298:175–180 CrossRefPubMed
Zurück zum Zitat Jacquin MF, Renehan WE, Mooney RD, Rhoades RW (1986) Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 55:1153–1186 CrossRefPubMed Jacquin MF, Renehan WE, Mooney RD, Rhoades RW (1986) Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 55:1153–1186 CrossRefPubMed
Zurück zum Zitat Jacquin MF, Renehan WE, Rhoades RW, Panneton WM (1993) Morphology and topography of identified primary afferents in trigeminal subnuclei principalis and oralis. J Neurophysiol 70:1911–1936 CrossRefPubMed Jacquin MF, Renehan WE, Rhoades RW, Panneton WM (1993) Morphology and topography of identified primary afferents in trigeminal subnuclei principalis and oralis. J Neurophysiol 70:1911–1936 CrossRefPubMed
Zurück zum Zitat Kaas JH, Florence SL, Jain N (1999) Subcortical contributions to massive cortical reorganizations. Neuron 22:657–660 CrossRefPubMed Kaas JH, Florence SL, Jain N (1999) Subcortical contributions to massive cortical reorganizations. Neuron 22:657–660 CrossRefPubMed
Zurück zum Zitat Kitahara Y, Ohta K, Hasuo H, Shuto T, Kuroiwa M, Sotogaku N, Togo A, Nakamura K, Nishi A (2016) Chronic fluoxetine induces the enlargement of perforant path-granule cell synapses in the mouse dentate gyrus. PLoS One 11:e0147307 CrossRefPubMedPubMedCentral Kitahara Y, Ohta K, Hasuo H, Shuto T, Kuroiwa M, Sotogaku N, Togo A, Nakamura K, Nishi A (2016) Chronic fluoxetine induces the enlargement of perforant path-granule cell synapses in the mouse dentate gyrus. PLoS One 11:e0147307 CrossRefPubMedPubMedCentral
Zurück zum Zitat Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24:628–633 CrossRefPubMed Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24:628–633 CrossRefPubMed
Zurück zum Zitat Kleinfeld D (2009) Vibrissa movement, sensation and sensorimotor control. In: Squire L, Albright T, Bloom F, Gage F, Spitzer N (eds) The New Encyclopedia of Neuroscience, Academic Press, Elsevier, London, pp 155–177 CrossRef Kleinfeld D (2009) Vibrissa movement, sensation and sensorimotor control. In: Squire L, Albright T, Bloom F, Gage F, Spitzer N (eds) The New Encyclopedia of Neuroscience, Academic Press, Elsevier, London, pp 155–177 CrossRef
Zurück zum Zitat Kobayashi Y, Matsumura G (1996) Central projections of primary afferent fibers from the rat trigeminal nerve labeled with isolectin B4-HRP. Neurosci Lett 217:89–92 CrossRefPubMed Kobayashi Y, Matsumura G (1996) Central projections of primary afferent fibers from the rat trigeminal nerve labeled with isolectin B4-HRP. Neurosci Lett 217:89–92 CrossRefPubMed
Zurück zum Zitat Koerber HR, Mirnics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655–3671 PubMed Koerber HR, Mirnics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655–3671 PubMed
Zurück zum Zitat LaMotte CC, Kapadia SE, Shapiro CM (1991) Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin- HRP (WGA-HRP). J Comp Neurol 311:546–562 CrossRefPubMed LaMotte CC, Kapadia SE, Shapiro CM (1991) Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin- HRP (WGA-HRP). J Comp Neurol 311:546–562 CrossRefPubMed
Zurück zum Zitat Landers MS, Knott GW, Lipp HP, Poletaeva I, Welker E (2011) Synapse formation in adult barrel cortex following naturalistic environmental enrichment. Neuroscience 199:143–152 CrossRefPubMed Landers MS, Knott GW, Lipp HP, Poletaeva I, Welker E (2011) Synapse formation in adult barrel cortex following naturalistic environmental enrichment. Neuroscience 199:143–152 CrossRefPubMed
Zurück zum Zitat Liu H, Llewellyn-Smith IJ, Basbaum AI (1995) Co-injection of wheat germ agglutinin-HRP and choleragenoid-HRP into the sciatic nerve of the rat blocks transganglionic transport. J Histochem Cytochem 43:489–495 CrossRefPubMed Liu H, Llewellyn-Smith IJ, Basbaum AI (1995) Co-injection of wheat germ agglutinin-HRP and choleragenoid-HRP into the sciatic nerve of the rat blocks transganglionic transport. J Histochem Cytochem 43:489–495 CrossRefPubMed
Zurück zum Zitat Machin R, Perez-Cejuela CG, Bjugn R, Avendano C (2006) Effects of long-term sensory deprivation on asymmetric synapses in the whisker barrel field of the adult rat. Brain Res 1107:104–110 CrossRefPubMed Machin R, Perez-Cejuela CG, Bjugn R, Avendano C (2006) Effects of long-term sensory deprivation on asymmetric synapses in the whisker barrel field of the adult rat. Brain Res 1107:104–110 CrossRefPubMed
Zurück zum Zitat Machín R, Blasco B, Bjugn R, Avendaño C (2004) The size of the whisker barrel field in adult rats: minimal nondirectional asymmetry and limited modifiability by chronic changes of the sensory input. Brain Res 1025:130–138 CrossRefPubMed Machín R, Blasco B, Bjugn R, Avendaño C (2004) The size of the whisker barrel field in adult rats: minimal nondirectional asymmetry and limited modifiability by chronic changes of the sensory input. Brain Res 1025:130–138 CrossRefPubMed
Zurück zum Zitat Maier DL, Grieb GM, Stelzner DJ, McCasland JS (2003) Large-scale plasticity in barrel cortex following repeated whisker trimming in young adult hamsters. Exp Neurol 184:737–745 CrossRefPubMed Maier DL, Grieb GM, Stelzner DJ, McCasland JS (2003) Large-scale plasticity in barrel cortex following repeated whisker trimming in young adult hamsters. Exp Neurol 184:737–745 CrossRefPubMed
Zurück zum Zitat Martin YB, Negredo P, Villacorta-Atienza JA, Avendano C (2014) Trigeminal intersubnuclear neurons: morphometry and input-dependent structural plasticity in adult rats. J Comp Neurol 522:1597–1617 CrossRefPubMed Martin YB, Negredo P, Villacorta-Atienza JA, Avendano C (2014) Trigeminal intersubnuclear neurons: morphometry and input-dependent structural plasticity in adult rats. J Comp Neurol 522:1597–1617 CrossRefPubMed
Zurück zum Zitat Miyoshi Y, Suemune S, Yoshida A, Takemura M, Nagase Y, Shigenaga Y (1994) Central terminations of low-threshold mechanoreceptive afferents in the trigeminal nuclei interpolaris and caudalis of the cat. J Comp Neurol 340:207–232 CrossRefPubMed Miyoshi Y, Suemune S, Yoshida A, Takemura M, Nagase Y, Shigenaga Y (1994) Central terminations of low-threshold mechanoreceptive afferents in the trigeminal nuclei interpolaris and caudalis of the cat. J Comp Neurol 340:207–232 CrossRefPubMed
Zurück zum Zitat Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673–682 CrossRefPubMed Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673–682 CrossRefPubMed
Zurück zum Zitat Nakagawa S, Kurata S, Yoshida A, Nagase Y, Moritani M, Takemura M, Bae YC, Shigenaga Y (1997) Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic elements. J Comp Neurol 389:12–33 CrossRefPubMed Nakagawa S, Kurata S, Yoshida A, Nagase Y, Moritani M, Takemura M, Bae YC, Shigenaga Y (1997) Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic elements. J Comp Neurol 389:12–33 CrossRefPubMed
Zurück zum Zitat Negredo P, Martin YB, Lagares A, Castro J, Villacorta JA, Avendano C (2009) Trigeminothalamic barrelette neurons: natural structural side asymmetries and sensory input-dependent plasticity in adult rats. Neuroscience 163:1242–1254 CrossRefPubMed Negredo P, Martin YB, Lagares A, Castro J, Villacorta JA, Avendano C (2009) Trigeminothalamic barrelette neurons: natural structural side asymmetries and sensory input-dependent plasticity in adult rats. Neuroscience 163:1242–1254 CrossRefPubMed
Zurück zum Zitat Nithianantharajah J, Levis H, Murphy M (2004) Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol Learn Mem 81:200–210 CrossRefPubMed Nithianantharajah J, Levis H, Murphy M (2004) Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol Learn Mem 81:200–210 CrossRefPubMed
Zurück zum Zitat Oszlacs O, Jancso G, Kis G, Dux M, Santha P (2015) Perineural capsaicin induces the uptake and transganglionic transport of choleratoxin B subunit by nociceptive C-fiber primary afferent neurons. Neuroscience 311:243–252 CrossRefPubMed Oszlacs O, Jancso G, Kis G, Dux M, Santha P (2015) Perineural capsaicin induces the uptake and transganglionic transport of choleratoxin B subunit by nociceptive C-fiber primary afferent neurons. Neuroscience 311:243–252 CrossRefPubMed
Zurück zum Zitat Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York
Zurück zum Zitat Rema V, Armstrong-James M, Jenkinson N, Ebner FF (2006) Short exposure to an enriched environment accelerates plasticity in the barrel cortex of adult rats. Neuroscience 140:659–672 CrossRefPubMedPubMedCentral Rema V, Armstrong-James M, Jenkinson N, Ebner FF (2006) Short exposure to an enriched environment accelerates plasticity in the barrel cortex of adult rats. Neuroscience 140:659–672 CrossRefPubMedPubMedCentral
Zurück zum Zitat Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. J Comp Neurol 252:154–174 CrossRefPubMed Rice FL, Mance A, Munger BL (1986) A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle-sinus complexes. J Comp Neurol 252:154–174 CrossRefPubMed
Zurück zum Zitat Robertson B, Perry MJ, Lawson SN (1991) Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J Neurocytol 20:387–395 CrossRefPubMed Robertson B, Perry MJ, Lawson SN (1991) Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J Neurocytol 20:387–395 CrossRefPubMed
Zurück zum Zitat Santha P, Jancso G (2003) Transganglionic transport of choleragenoid by capsaicin-sensitive C-fibre afferents to the substantia gelatinosa of the spinal dorsal horn after peripheral nerve section. Neuroscience 116:621–627 CrossRefPubMed Santha P, Jancso G (2003) Transganglionic transport of choleragenoid by capsaicin-sensitive C-fibre afferents to the substantia gelatinosa of the spinal dorsal horn after peripheral nerve section. Neuroscience 116:621–627 CrossRefPubMed
Zurück zum Zitat Shehab SAS, Hughes DI (2011) Simultaneous identification of unmyelinated and myelinated primary somatic afferents by co-injection of isolectin B4 and Cholera toxin subunit B into the sciatic nerve of the rat. J Neurosci Methods 198:213–221 CrossRefPubMed Shehab SAS, Hughes DI (2011) Simultaneous identification of unmyelinated and myelinated primary somatic afferents by co-injection of isolectin B4 and Cholera toxin subunit B into the sciatic nerve of the rat. J Neurosci Methods 198:213–221 CrossRefPubMed
Zurück zum Zitat Shehab SAS, Spike RC, Todd AJ (2003) Evidence against cholera toxin B subunit as a reliable tracer for sprouting of primary afferents following peripheral nerve injury. Brain Res 964:218–227 CrossRefPubMed Shehab SAS, Spike RC, Todd AJ (2003) Evidence against cholera toxin B subunit as a reliable tracer for sprouting of primary afferents following peripheral nerve injury. Brain Res 964:218–227 CrossRefPubMed
Zurück zum Zitat Shortland PJ, Demaro JA, Jacquin MF (1995) Trigeminal structure-function relationships: a reevaluation based on long-range staining of a large sample of brainstem A beta fibers. Somatosens Motor Res 12:249–275 CrossRef Shortland PJ, Demaro JA, Jacquin MF (1995) Trigeminal structure-function relationships: a reevaluation based on long-range staining of a large sample of brainstem A beta fibers. Somatosens Motor Res 12:249–275 CrossRef
Zurück zum Zitat Shortland PJ, Demaro JA, Shang F, Waite PME, Jacquin MF (1996) Peripheral and central predictors of whisker afferent morphology in the rat brainstem. J Comp Neurol 375:481–501 CrossRefPubMed Shortland PJ, Demaro JA, Shang F, Waite PME, Jacquin MF (1996) Peripheral and central predictors of whisker afferent morphology in the rat brainstem. J Comp Neurol 375:481–501 CrossRefPubMed
Zurück zum Zitat Shortland P, Kinman E, Molander C (1997) Sprouting of A-fibre primary afferents into lamina II in two rat models of neuropathic pain. Eur J Pain 1:215–227 CrossRefPubMed Shortland P, Kinman E, Molander C (1997) Sprouting of A-fibre primary afferents into lamina II in two rat models of neuropathic pain. Eur J Pain 1:215–227 CrossRefPubMed
Zurück zum Zitat Silverman JD, Kruger L (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 19:789–801 CrossRefPubMed Silverman JD, Kruger L (1990) Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 19:789–801 CrossRefPubMed
Zurück zum Zitat Tong YG, Wang HF, Ju G, Grant G, Hökfelt T, Zhang X (1999) Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J Comp Neurol 404:143–158 CrossRefPubMed Tong YG, Wang HF, Ju G, Grant G, Hökfelt T, Zhang X (1999) Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J Comp Neurol 404:143–158 CrossRefPubMed
Zurück zum Zitat West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497 CrossRefPubMed West MJ, Slomianka L, Gundersen HJG (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497 CrossRefPubMed
Zurück zum Zitat Willis WDJ, Coggeshall RE (2004) Sensory mechanisms of the spinal cord. Vol. 1. Primary afferent neurons and the spinal dorsal horn, vol 1. Kluwer/Plenum, New York Willis WDJ, Coggeshall RE (2004) Sensory mechanisms of the spinal cord. Vol. 1. Primary afferent neurons and the spinal dorsal horn, vol 1. Kluwer/Plenum, New York
Zurück zum Zitat Woodbury CJ, Kullmann FA, McIlwrath SL, Koerber HR (2008) Identity of myelinated cutaneous sensory neurons projecting to nocireceptive laminae following nerve injury in adult mice. J Comp Neurol 508:500–509 CrossRefPubMedPubMedCentral Woodbury CJ, Kullmann FA, McIlwrath SL, Koerber HR (2008) Identity of myelinated cutaneous sensory neurons projecting to nocireceptive laminae following nerve injury in adult mice. J Comp Neurol 508:500–509 CrossRefPubMedPubMedCentral
Zurück zum Zitat Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75–78 CrossRefPubMed Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75–78 CrossRefPubMed
Zurück zum Zitat Woolf CJ, Shortland P, Reynolds M, Ridings J, Doubell T, Coggeshall RE (1995) Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol 360:121–134 CrossRefPubMed Woolf CJ, Shortland P, Reynolds M, Ridings J, Doubell T, Coggeshall RE (1995) Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol 360:121–134 CrossRefPubMed
Zurück zum Zitat Zhang Y, Chen Y, Liedtke W, Wang F (2015) Lack of evidence for ectopic sprouting of genetically labeled Abeta touch afferents in inflammatory and neuropathic trigeminal pain. Mol Pain 11:18-0017 Zhang Y, Chen Y, Liedtke W, Wang F (2015) Lack of evidence for ectopic sprouting of genetically labeled Abeta touch afferents in inflammatory and neuropathic trigeminal pain. Mol Pain 11:18-0017
Metadaten
Titel
Changes in the axon terminals of primary afferents from a single vibrissa in the rat trigeminal nuclei after active touch deprivation or exposure to an enriched environment
verfasst von
Julia Fernández-Montoya
Yasmina B. Martin
Pilar Negredo
Carlos Avendaño
Publikationsdatum
12.07.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 1/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1472-5

Weitere Artikel der Ausgabe 1/2018

Brain Structure and Function 1/2018 Zur Ausgabe

Neu im Fachgebiet Neurologie

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Neurologie und bleiben Sie gut informiert – ganz bequem per eMail.