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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

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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.

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Abbreviations

ABC:

Avidin-biotynilated peroxidase complex

Cb:

Cerebellum

CE:

Coefficient of error

CTB:

Cholera toxin, fraction B

DAB:

3,3′-Diaminobenzidine

DVN:

Deep vibrissal nerve

DRG:

Dorsal root ganglion

HRP:

Horseradish peroxidase

IB4:

Isolectin B4 from Griffoniasimplicifolia

IoN:

Infraorbital nerve

PB:

Phosphate buffer

Pr5:

Principal trigeminal nucleus

Sp5c:

Spinal trigeminal nucleus, pars caudalis

Sp5ip:

Spinal trigeminal nucleus, pars interpolaris

Sp5o:

Spinal trigeminal nucleus, pars oralis

t5:

Spinal trigeminal tract

TG:

Trigeminal ganglion

WGA:

Wheat germ agglutinin

References

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown AG (1981) Organization in the spinal cord. The anatomy and physiology of identified neurones. Springer, Berlin

    Google Scholar 

  • Bush NE, Solla SA, Hartmann MJ (2016) Whisking mechanics and active sensing. Curr Opin Neurobiol 40:178–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cruz-Orive LM (1999) Precision of Cavalieri sections and slices with local errors. J Microsc 193:182–198

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Diamond MC (1988) Enriching heredity. The impact of the environment on the anatomy of the brain. The Free Press, London

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ebner FF (2005) Neural plasticity in adult somatic sensory-motor systems. Taylor & Francis/CRC Press, Boca Raton

    Book  Google Scholar 

  • Federmeier KD, Kleim JA, Greenough WT (2002) Learning-induced multiple synapse formation in rat cerebellar cortex. Neurosci Lett 332:180–184

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Fox K, Wong RO (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48:465–477

    Article  CAS  PubMed  Google Scholar 

  • Froemke RC (2015) Plasticity of cortical excitatory-inhibitory balance. Annu Rev Neurosci 38:195–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frostig RD (2006) Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr Opin Neurobiol 16:445–450

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gogolla N, Galimberti I, Caroni P (2007) Structural plasticity of axon terminals in the adult. Curr Opin Neurobiol 17:516–524

    Article  CAS  PubMed  Google Scholar 

  • Gundersen HJG (1988) The nucleator. J Microsc 151:3–21

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior. A neuropsychological theory. Wiley, New York

    Google Scholar 

  • Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10:647–658

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jacquin MF, Rhoades RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Motor Res 7:265–288

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kaas JH, Florence SL, Jain N (1999) Subcortical contributions to massive cortical reorganizations. Neuron 22:657–660

    Article  CAS  PubMed  Google Scholar 

  • Katzel D, Miesenbock G (2014) Experience-dependent rewiring of specific inhibitory connections in adult neocortex. PLoS Biol 12:e1001798

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirkman TW (1996) Statistics to use. pp 1–9. http://www.physics.csbsju.edu/stats/. Accessed 4 Nov 2015

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Koerber HR, Mirnics K, Brown PB, Mendell LM (1994) Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci 14:3655–3671

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Larsen JO (1998) Stereology of nerve cross sections. J Neurosci Methods 85:107–118

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673–682

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75–78

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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Acknowledgements

The authors gratefully acknowledge Ms. Begoña Rodriguez for her skilled technical help in the preparation of the histological material, and the Servicios de Microscopía Confocal and Microscopía Electrónica de Transmisión of the SIDI-UAM for their help in the confocal microscopy analyses. We also thank Dr. A. Krzyzanowska for reading a final draft of the manuscript and making useful style suggestions. This study was supported by Grants BFU2012-39960 and BFU2015-66941R from Spain’s Ministerio de Economía Industria y competitividad/Fondo Europeo de Desarrollo Regional (MINECO/FEDER).

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  1. Julia Fernández-Montoya and Yasmina B. Martin contributed equally to this work.

Authors and Affiliations

  1. Department of Anatomy, Histology and Neuroscience, Medical School, Autonoma University of Madrid, c/Arzobispo Morcillo 2, 28029, Madrid, Spain

    Julia Fernández-Montoya, Pilar Negredo & Carlos Avendaño

  2. Departamento de Anatomía, Facultad de Ciencias de la Salud, Universidad Francisco de Vitoria, UFV, Edificio E, Ctra. M-115, Pozuelo-Majadahonda Km 1,800, Pozuelo de Alarcón, 28223, Madrid, Spain

    Yasmina B. Martin

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Correspondence to Carlos Avendaño.

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429_2017_1472_MOESM1_ESM.tif

Fig. 1:Injection of CTB and IB4 in a single deep vibrissal nerve (DVN). (a) Exposure of the deep nerve from vibrissal follicle C1. Star, follicle; arrows, stretch of the nerve attaching to the follicle wall. (b) Intraneural deposit of a mixture of tracers with Light Green to help visualization of the same nerve; the picture was taken immediately after finishing the injection. (c) Confocal immunofluorescence image of a cross section of C1 DVN, 2 mm proximal to the injection. Most, if not all, medium-sized and large axons are labeled by CTB (red). Asterisk marks a blood vessel artifact. (d) Semithin section of C1 DVN injected with both tracers, subjected to a preembedding immunohistochemistry and counterstained with toluidine blue. The axoplasm of most myelinated axons, normally unstained by toluidine blue, exhibits now a dark color due to the immunoreaction. (e) Low-power electron micrograph of a cross section of C1 DVN in a naïve case without injection of tracers. (f, g) High power electron micrographs of the same C1 DVN as in (d), showing details of several labeled myelinated and unmyelinated axons. The axoplasm of myelinated axons seems uniformly filled with a diffuse precipitate which masks the axonal cytoskeleton. Unmyelinated axons are irregularly filled with dark deposits (arrows). Scale bars 200 µm (a, b), 20 µm (c), 50 µm (d, e), and 2 µm (f, g) (TIFF 42358 kb)

429_2017_1472_MOESM2_ESM.tif

Fig. 2: Panels showing examples of neuron somata in the TG of a control case that are single-labeled by either CTB (a, b, c: red, left boxes of each panel) or IB4 (a, b, c: green, middle boxes). Merged images in the boxes on the right show no colocalization of the tracers. In (c), however, a few small neurons in the same case show colocalization (arrowheads). Scale bars: 40 µm (TIFF 19353 kb)

429_2017_1472_MOESM3_ESM.tif

Fig. 3: Confocal merged images with orthogonal projections showing three examples of varicosities double-labeled for CTB (red) and IB4 (green) in lamina II of Sp5c in a control case. (a) Example of a fairly large double-labeled varicosity (arrow) located very close to another varicosity that is only labeled for CTB. (b, c) Crosshairs marking two small double-labeled profiles, probably corresponding to small varicosities. Scale bars 50 µm (a), 10 µm (b, c) (TIFF 20286 kb)

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Fernández-Montoya, J., Martin, Y.B., Negredo, P. et al. 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. Brain Struct Funct 223, 47–61 (2018). https://doi.org/10.1007/s00429-017-1472-5

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