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Structure-function relationships in identified afferent neurones

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Summary

The review deals with structure-function relationships in primary afferent and spinal cord neurones that were intracellularly injected with a marker substance (mostly HRP) after physiological identification. At the level of dorsal root ganglion (DRG) cells, there is a significant correlation between soma size and conduction velocity (or diameter) of the afferent fibre for most subpopulations of DRG cells, but the scatter of data is considerable, so that the size of a DRG cell soma cannot be predicted from the diameter of its axon or vice versa. The spinal terminations of primary afferent fibres are the best example of a relationship between structure and function, since most of the afferent units possess characteristic patterns of spinal arborization, e.g. the “flame-shaped arbors” of hair follicle afferents in lamina III of the dorsal horn, or the projection of nociceptive afferents onto lamina I. The morphological features of spinal cord neurones can be used only to a limited extent for functional identification. Thus, many SCT neurones can be recognized by their triangular dendritic tree and STT cells in lamina VII/VIII by their dendritic projection into the white matter. It is still not possible, however, to distinguish a nociceptive STT cell from a low-threshold mechanoreceptive one on the basis of morphological criteria.

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References

  • Abrahams VC, Richmond FJR, Keane J (1984) Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: a study using transganglionic transport of horseradish peroxidase. J Comp Neurol 230:142–154

    Google Scholar 

  • Ammann B, Gottschall J, Zenker W (1983) Afferent projections from the rat longus capitis muscle studied by transganglionic transport of HRP. Anat Embryol 166:275–289

    Google Scholar 

  • Andres KH (1961) Untersuchungen über den Feinbau von Spinalganglien. Z Zellforsch 55:1–48

    Google Scholar 

  • Bahr R, Blumberg H, Jänig W (1981) Do dichotomizing afferent fibers exist which supply visceral organs as well as somatic structures? A contribution to the problem of referred pain. Neurosci Lett 24:25–28

    Google Scholar 

  • Bakker DA, Richmond FJR, Abrahams VC (1984) Central projections from cat suboccipital muscles: a study using transganglionic transport of horseradish peroxidase. J Comp Neurol 228:409–421

    Google Scholar 

  • Basbaum AI, Fields HL (1984) Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Ann Rev Neurosci 7:309–338

    Google Scholar 

  • Bennett GJ, Hayashi H, Abdelmoumene M, Dubner R (1979) Physiological properties of stalked cells of the substantia gelatinosa intracellularly stained with horseradish peroxidase. Brain Res 164:285–289

    Google Scholar 

  • Bennett GJ, Abdelmoumene M, Hayashi H, Dubner R (1980) Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase. J Comp Neurol 194:809–827

    Google Scholar 

  • Bennett GJ, Nishikawa N, Guo-Wei Lu, Hoffert MJ, Dubner R (1984) The morphology of dorsal column postsynaptic spinomedullary neurons in the cat. J Comp Neurol 224:568–578

    Google Scholar 

  • Brown AG (1981) Organization in the spinal cord. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Brown AG, Fyffe REW (1978) The morphology of group Ia afferent fibre collaterals in the spinal cord of the cat. J Physiol 274:111–127

    Google Scholar 

  • Brown AG, Fyffe REW (1981a) Direct observations on the contacts made between Ia afferent fibres and alpha-motoneurones in the cat's lumbosacral spinal cord. J Physiol 313:121–140

    Google Scholar 

  • Brown AG, Fyffe REW (1981b) Form and function of dorsal horn neurones with axons ascending the dorsal columns in cat. J Physiol 321:31–47

    Google Scholar 

  • Brown AG, Fyffe REW (1984) Intracellular staining of mammalian neurones. Academic Press, London

    Google Scholar 

  • Brown AG, Noble R (1982) Connexions between hair follicle afferent fibres and spinocervical tract neurones in the cat: the synthesis of receptive fields. J Physiol 323:77–91

    Google Scholar 

  • Brown AG, House CR, Rose PK, Snow PJ (1976) The morphology of spinocervical tract neurones in the cat. J Physiol 260:719–738

    Google Scholar 

  • Brown AG, Rose PK, Snow PJ (1977a) The morphology of spinocervical tract neurones revealed by intracellular injection of horseradish peroxidase. J Physiol 270:747–765

    Google Scholar 

  • Brown AG, Rose PK, Snow PJ (1977b) The morphology of hair follicle afferent fibre collaterals in the spinal cord of the cat. J Physiol 272:779–797

    Google Scholar 

  • Brown AG, Fyffe REW, Noble R (1980) Projections from Pacinian corpuscles and rapidly adapting mechanoreceptors of glabrous skin to the cat's spinal cord. J Physiol 307:385–400

    Google Scholar 

  • Brown AG, Fyffe REW, Rose PK, Snow PJ (1981) Spinal cord collaterals from axons of type II slowly adapting units in the cat. J Physiol 316:469–480

    Google Scholar 

  • Buck SH, Walsh JH, Yamamura HI, Burks TF (1982) Neuropeptides in sensory neurons. Life Sci 30:1857–1866

    Google Scholar 

  • Cameron AA, Leah JD, Snow PJ (1986) The electrophysiological and morphological characteristics of feline dorsal root ganglion cells. Brain Res 362:1–6

    Google Scholar 

  • Carstens E, Trevino DL (1978) Anatomical and physiological properties of ipsilaterally projecting spinothalamic neurons in the second cervical segment of the cat's spinal cord. J Comp Neurol 182:167–184

    Google Scholar 

  • Cervero F, Connell LA (1984) Distribution of somatic and visceral primary afferent fibres within the thoracic spinal cord of the cat. J Comp Neurol 230:88–98

    Google Scholar 

  • Cervero F, Iggo A (1980) The substantia gelatinosa of the spinal cord. A critical review. Brain 103:717–772

    Google Scholar 

  • Chung K, Coggeshall RE (1984) The ratio of dorsal root ganglion cells to dorsal root axons in sacral segments of the cat. J Comp Neurol 225:24–30

    Google Scholar 

  • Craig AD, Mense S (1983) The distribution of afferent fibres from the gastrocnemius-soleus muscle in the dorsal horn of the cat, as revealed by the transport of horseradish peroxidase. Neurosci Lett 41:233–238

    Google Scholar 

  • Cruz F, Lima D, Coimbra A (1987) Several morphological types of terminal arborizations of primary afferents in laminae I–II of the rat spinal cord, as shown after HRP labeling and Golgi impregnation. J Comp Neurol 261:221–236

    Google Scholar 

  • Cullheim S, Kellerth J-O (1976) Combined light and electron microscopic tracing of neurons, including axons and synaptic terminals, after intracellular injection of horseradish peroxidase. Neurosci Lett 2:307–313

    Google Scholar 

  • Dembowsky K, Czachurski J, Seller H (1985a) An intracellular study of the synaptic input to sympathetic preganglionic neurones of the third thoracic segment of the cat. J Auton Nerv Syst 13:201–244

    Google Scholar 

  • Dembowsky K, Czachurski J, Seller H (1985b) Morphology of sympathetic preganglionic neurons in the thoracic spinal cord of the cat: an intracellular horseradish peroxidase study. J Comp Neurol 238:453–465

    Google Scholar 

  • Devor M, Wall PD, McMahon SB (1984) Dichotomizing somatic nerve fibers exist in rats but they are rare. Neurosci Lett 49:187–192

    Google Scholar 

  • Dubner R, Ruda MA, Miletic V, Hoffert MJ, Bennett GJ, Nishikawa N, Coffield J (1984) Neural circuitry mediating nociception in the medullary and spinal dorsal horns. In: Kruger L, Liebeskind JC (eds) Advances in pain research and therapy, vol. 6. Raven Press, New York, pp 151–166

    Google Scholar 

  • Fyffe REW (1979) The morphology of group II muscle afferent fibre collaterals. J Physiol 296:39P-40P

    Google Scholar 

  • Gallego R, Eyzaguirre C (1978) Membrane and action potential characteristics of A and C nodose ganglion cells studied in whole ganglia and in tissue slices. J Neurophysiol 41:1217–1232

    Google Scholar 

  • Gilette R, Pomeranz B (1973) Neuron geometry and circuitry via the electron microscope: intracellular staining with osmiophilic polymer. Science 182:1256–1258

    Google Scholar 

  • Globus A, Lux HD, Schubert P (1968) Somadendritic spread of intracellularly injected tritiated glycine in cat spinal motoneurons. Brain Res 11:440–445

    Google Scholar 

  • Gobel S (1978a) Golgi studies of the neurons in layer I of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:375–394

    Google Scholar 

  • Gobel S (1978b) Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:395–414

    Google Scholar 

  • Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359:31–46

    Google Scholar 

  • Hökfelt T, Johansson O, Ljungdahl A, Lundberg JM, Schultzberg M (1980) Peptidergic neurones. Nature 284:515–521

    Google Scholar 

  • Hoffert MJ, Miletic V, Ruda MA, Dubner R (1983) Immunocytochemical identification of serotonin axonal contacts on characterized neurons in laminae I and II of the cat dorsal horn. Brain Res 267:361–364

    Google Scholar 

  • Hoheisel U, Mense S (1987) Observations on the morphology of axons and somata of slowly conducting dorsal root ganglion cells in the cat. Brain Res 423:269–278

    Google Scholar 

  • Hoheisel U, Lehmann-Willenbrock E, Mense S (1989) Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat. Neurosci 28:495–507

    Google Scholar 

  • Honda CN, Lee CL (1985) Immunochemistry of synaptic input and functional characterizations of neurons near the spinal central canal. Brain Res 343:120–128

    Google Scholar 

  • Honda CN, Perl ER (1985) Functional and morphological features of neurons in the midline region of the caudal spinal cord of the cat. Brain Res 340:285–295

    Google Scholar 

  • Hongo T, Kudo N, Yamashita M, Ishizuka N, Mannen H (1981) Transneuronal passage of intraaxonally injected horseradish peroxidase (HRP) from group Ib and II fibers into the secondary neurons in the dorsal horn of the cat spinal cord. Biomed Res 2:722–727

    Google Scholar 

  • Hongo T, Kudo N, Sasaki S, Yamashita M, Yoshida K, Ishizuka N, Mannen H (1987) Trajectory of group Ia and Ib fibers from the hindlimb muscles at the L3 and L4 segments of the spinal cord of the cat. J Comp Neurol 262:159–194

    Google Scholar 

  • Hughes AFW (1968) Aspects of neural ontogeny. Academic Press, London

    Google Scholar 

  • Hursh JB (1939) Conduction velocity and diameter of nerve fibers. Amer J Physiol 127:131–139

    Google Scholar 

  • Hylden JK, Hayashi H, Ruda MA, Dubner R (1986) Serotonin innervation of physiologically identified lamina I projection neurons. Brain Res 370:401–404

    Google Scholar 

  • Ishizuka N, Mannen H, Hongo T, Sasaki S (1979) Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: three dimensional reconstructions from serial sections. J Comp Neurol 186:189–212

    Google Scholar 

  • Jacobson M (1969) Development of specific neuronal connections. Science 163:543–547

    Google Scholar 

  • Jankowska E, Lindström S (1970) Morphological identification of physiologically defined neurones in the cat spinal cord. Brain Res 20:323–326

    Google Scholar 

  • Jankowska E, Rastad J, Westman J (1976) Intracellular application of horseradish peroxidase and its light and electron microscopical appearance in spinocervical tract cells. Brain Res 105:557–562

    Google Scholar 

  • Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer JA, Frey P (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin- immunoreactive ganglion cells. Cell Tissue Res 247:417–431

    Google Scholar 

  • Kitai ST, Kocsis JD, Preston RJ, Sugimori M (1976) Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase. Brain Res 109:601–606

    Google Scholar 

  • Koerber HR, Brown PB (1980) Projections of two hindlimb cutaneous nerves to cat dorsal horn. J Neurophysiol 44:259–269

    Google Scholar 

  • Kuo DC, Nadelhaft I, Hisamitsu T, deGroat WC (1983) Segmental distribution and central projections of renal afferent fibers in the cat studied by transganglionic transport of horseradish peroxidase. J Comp Neurol 216:162–174

    Google Scholar 

  • LaMotte C (1977) Distribution of the tract of Lissauer and the dorsal root fibers in the primate spinal cord. J Comp Neurol 172:529–562

    Google Scholar 

  • Langford LA, Coggeshall RE (1979) Branching of sensory axons in the dorsal root and evidence for the absence of dorsal root efferent fibers. J Comp Neurol 184:193–204

    Google Scholar 

  • Langford LA, Coggeshall RE (1981) Branching of sensory axons in the peripheral nerve of the rat. J Comp Neurol 203:745–750

    Google Scholar 

  • Laurberg S, Sørensen KE (1985) Cervical dorsal root ganglion cells with collaterals to both shoulder skin and the diaphragm. A fluorescent double labelling study in the rat. A model for referred pain? Brain Res 331:160–163

    Google Scholar 

  • Lawson SN, Harper AA, Harper EI, Garson JA, Anderton BH (1984) A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones. J Comp Neurol 228:263–272

    Google Scholar 

  • Leah JD, Cameron AA, Kelly WL, Snow PJ (1985a) Coexistence of peptide immunoreactivity in sensory neurons of the cat. Neurosci 16:683–690

    Google Scholar 

  • Leah JD, Cameron AA, Snow PJ (1985b) Neuropeptides in physiologically identified mammalian sensory neurones. Neurosci Lett 56:257–263

    Google Scholar 

  • Lee KH, Chung K, Chung JM, Coggeshall RE (1986) Correlation of cell body size, axon size, and signal conduction velocity for individually labelled dorsal root ganglion cells in the rat. J Comp Neurol 243:335–346

    Google Scholar 

  • Lieberman AR (1976) Sensory ganglia. In: Landon DN (ed) The peripheral nerve. Wiley, New York, pp 188–278

    Google Scholar 

  • Light AR (1985) The spinal terminations of single, physiologically characterized axons originating in the pontomedullary raphe of the cat, J Comp Neurol 234:536–548

    Google Scholar 

  • Light AR, Durkovic RG (1976) Horseradish peroxidase: an improvement in intracellular staining of single, electrophysiologically characterized neurons. Exp Neurol 53:847–853

    Google Scholar 

  • Light AR, Perl ER (1977) Differential termination of large-diameter and small-diameter primary afferent fibers in the spinal dorsal grey matter as indicated by labeling with horseradish peroxidase. Neurosci Lett 6:59–63

    Google Scholar 

  • Light AR, Perl ER (1979) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133–150

    Google Scholar 

  • Light AR, Trevino DL, Perl ER (1979) Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J Comp Neurol 186:151–171

    Google Scholar 

  • Maxwell DJ, Koerber HR (1987) Morphologically unusual feline spinocervical tract neurons. Exp Neurol 95:521–524

    Google Scholar 

  • Maxwell DJ, Koerber HR, Bannatyne BA (1985) Light and electron microscopy of contacts between primary afferent fibres and neurones with axons ascending the dorsal columns of the feline spinal cord. Neurosci 16:375–394

    Google Scholar 

  • Maxwell DJ, Réthelyi M (1987) Ultrastructure and synaptic connections of cutaneous afferent fibres in the spinal cord. Trends Neurosci 10:117–122

    Google Scholar 

  • Mense S, Craig AD (1988) Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat. Neuroscience 26:1023–1035

    Google Scholar 

  • Mense S, Prabhakar NR (1986) Spinal termination of nociceptive afferent fibres from deep tissues in the cat. Neurosci Lett 66:169–174

    Google Scholar 

  • Mense S, Light AR, Perl ER (1981) Spinal terminations of subcutaneous high-threshold mechanoreceptors. In: Brown AG, Réthelyi M (eds) Spinal cord sensation. Scottish Academic Press, Edinburgh, pp 79–86

    Google Scholar 

  • Mense S, Craig AD, Lehmann-Willenbrock E, Meyer H (1985) Neurobiology of small-diameter afferent fibers from deep tissues. In: Willis WD, Rowe MJ (eds) Development, organisation and processing in somatosensory pathways. Alan Liss, New York, pp 299–308

    Google Scholar 

  • Meyers DER, Snow PJ (1982a) The response to somatic stimuli of deep spinothalamic tract cells in the lumbar spinal cord of the cat. J Physiol 329:355–371

    Google Scholar 

  • Meyers DER. Snow PJ (1982b) The morphology of physiologically identified deep spinothalamic tract cells in the lumbar spinal cord of the cat. J Physiol 329:373–388

    Google Scholar 

  • Meyers DER, Snow PJ (1984) Somatotopically inappropriate projections of single hair follicle afferent fibres to the cat spinal cord. J Physiol 347:59–73

    Google Scholar 

  • Mysicka A, Zenker W (1981) Central projections of muscle afferents from the sternomastoid nerve in the rat. Brain Res 211:257–265

    Google Scholar 

  • Nahin RL, Madsen AM, Giesler GJ (1983) Anatomical and physiological studies of the gray matter surrounding the spinal cord central canal. J Comp Neurol 220:321–335

    Google Scholar 

  • Nyberg G, Blomqvist A (1984) The central projection of muscle afferent fibres to the lower medulla and upper spinal cord: An anatomical study in the cat with the transganglionic transport method. J Comp Neurol 230:99–109

    Google Scholar 

  • Oehme P, Krivoy WA (1983) Substance P: a peptide with unusual features. Trends Pharmacol Sci 4:521–523

    Google Scholar 

  • Oku R, Satoh M, Takagi H (1987) Release of substance P from the spinal dorsal horn is enhanced in polyarthritic rats. Neurosci Lett 74:315–319

    Google Scholar 

  • Petras JM, Cummings JF (1972) Autonomic neurons in the spinal cord of the rhesus monkey: a correlation of the findings of cytoarchitectonics and sympathectomy with fiber degeneration following dorsal rhizotomy. J Comp Neurol 146:189–218

    Google Scholar 

  • Pierau F-K, Taylor DCM, Abel W, Friedrich B (1982) Dichotomizing peripheral fibres revealed by intracellular recording from rat sensory neurones. Neurosci Lett 31:123–128

    Google Scholar 

  • Ralston HJ, Ralston DD (1979) The distribution of dorsal root axons in laminae I, II and III of the Macaque spinal cord: A quantitative electron microscope study. J Comp Neurol 184:643–684

    Google Scholar 

  • Ranson SW (1912) The structure of the spinal ganglia and of the spinal nerves. J Comp Neurol 22:159–175

    Google Scholar 

  • Réthelyi M (1972) Cell and neuropil architecture of the intermediolateral (sympathetic) nucleus of cat spinal cord. Brain Res 46:203–213

    Google Scholar 

  • Rexed B (1952) The cytoarchitectonic organization of the spinal cord in the rat. J Comp Neurol 96:415–496

    Google Scholar 

  • Scheibel ME, Scheibel AB (1968) Terminal axonal patterns in cat spinal cord. II. The dorsal horn. Brain Res 9:32–58

    Google Scholar 

  • Semba K, Masarchia P, Malamed S, Jacquin M, Harris S, Yang G, Egger MD (1985) An electron microscopic study of terminals of rapidly adapting mechanoreceptive afferent fibers in the cat spinal cord. J Comp Neurol 232:229–240

    Google Scholar 

  • Sinclair DC, Weddell G, Feindel WH (1948) Referred pain and associated phenomena. Brain 71:184–211

    Google Scholar 

  • Snow PJ, Rose PK, Brown AG (1976) Tracing axons and axon collaterals of spinal neurons using intracellular injection of horseradish peroxidase. Science 191:312–313

    Google Scholar 

  • Stretton AOW, Kravitz EA (1968) Neuronal geometry: determination with a technique of intracellular dye injection. Science 162:132–134

    Google Scholar 

  • Sugiura Y, Lee CL, Perl ER (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234:358–361

    Google Scholar 

  • Taylor DCM, Pierau F-K (1982) Double fluorescence labelling supports electrophysiological evidence for dichotomizing peripheral sensory nerve fibres in rats. Neurosci Lett 33:1–6

    Google Scholar 

  • Thomas RC, Wilson UJ (1966) Marking single neurons by staining with intracellular recording electrodes. Science 151:1538–1539

    Google Scholar 

  • Tracey DJ, Walmsley B (1984) Synaptic input from identified muscle afferents to neurones of the dorsal spinocerebellar tract in the cat. J Physiol 350:599–614

    Google Scholar 

  • Wall PD (1977) The presence of ineffective synapses and circumstances which unmask them. Philos Trans R Soc Lond B 278:361–372

    Google Scholar 

  • Willis WD, Kenshalo DR, Leonard RB (1979) The cells of origin of the primate spinothalamic tract. Comp Neurol 188:543–574

    Google Scholar 

  • Yoshida S, Matsuda Y (1979) Studies on sensory neurons of the mouse with intracellular-recording and horseradish peroxidase-injection techniques. J Neurophysiol 42:1134–1145

    Google Scholar 

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  1. Institut für Anatomie und Zellbiologie, Universität Heidelberg, Im Neuenheimer Feld 307, D-6900, Heidelberg, Federal Republic of Germany

    S. Mense

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Mense, S. Structure-function relationships in identified afferent neurones. Anat Embryol 181, 1–17 (1990). https://doi.org/10.1007/BF00189723

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