9 - Development of the somatosensory system  pp. 129-146

Development of the somatosensory system

By Sandra Rees, David Walker and Ernest Jennings

Image View Previous Chapter Next Chapter



Introduction

The somatosensory system deals with information from a variety of sensory receptors located in the skin, muscles, joints, and other deeper tissues. It enables us to experience touch, pain, warmth, and cold, and to sense the position and movements of our body. Understanding how this system develops structurally and functionally during embryonic and fetal life provides an insight into how the fetus and newborn infant develops the capacity to receive and experience sensations arising from noxious, tactile, thermal, or mechanical stimuli. Although it will be difficult to determine, unequivocally, when the fetus is first aware of its surroundings and conscious of perceiving these stimuli, we can at least define when the minimum structural and functional apparatus necessary to do so is present.

In this chapter we will first describe the structure of the main pathways that transmit tactile, thermal, nociceptive, and proprioceptive information from the periphery to the cerebral cortex via synaptic connections in the spinal cord or brainstem. We will then describe the structural, neurochemical, and functional development of the somatosensory system and the development of descending pathways from the brainstem which modify this activity. We will speculate on whether activity in the fetal somatosensory pathways is a necessary requirement for the appropriate development of these pathways as it appears to be for the visual system (Goodman & Shatz, 1993; Penn & Shatz, 1999). Clearly, very little experimentation can be performed on the human fetus, and laboratory animals are therefore used to answer these questions.

Abdel-Majid, R. M. , Leong, W. L. , Schalkwyk, L. C. , et al. (1998). Loss of adenyl cyclase I activity disrupts the patterning of mouse somatosensory cortex. Nature Genetics, 19, 289–91.
Acheson, A. , Conover, J. C. , Fandl, J. P. , et al. (1995). A BDNF autocrine loop in adult sensory neurons prevents cell death [see comments]. Nature, 374, 450–3.
Allendoerfer, K. L . & Shatz, C. J . (1994). The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annual Review of Neuroscience, 17, 185–218.
Altman, J . & Bayer, S. A . (1979). Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. Journal of Comparative Neurology, 188, 455–71.
Andrews, K . & Fitzgerald, M . (1994). The cutaneous withdrawal reflex in human neonates: sensitization, receptive fields, and the effects of contralateral stimulation. Pain, 56, 95–101.
Andrews, K . & Fitzgerald, M . (1999). Cutaneous flexion reflex in human neonates: a quantitative study of threshold and stimulus-response characteristics after single and repeated stimuli. Developmental Medicine and Child Neurology, 41, 696–703.
Baccei, M. L . & Fitzgerald, M . (2004). Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. Journal of Neuroscience, 24, 4749–57.
Baccei, M. L. , Bardoni, R. , & Fitzgerald, M. (2003). Development of nociceptive synaptic inputs to the neonatal rat dorsal horn: glutamate release by capsaicin and menthol. Journal of Physiology, 549, 231–42.
Barker, D . & A. Milburn (1984). Development and regeneration of mammalian muscle spindles. Science Progress, 69, 45–64.
Bartocci, M. , Bergqvist, L. L. , Lagercrantz, H. , et al. (2006). Pain activates cortical areas in the preterm newborn. Pain, 122, 109–17.
Bregman, B. S . (1987). Development of serotonin immunoreactivity in the rat spinal cord and its plasticity after neonatal spinal cord lesions. Brain Research, 431, 245–63.
Catalano, S. M . & Shatz, C. J . (1998). Activity-dependent cortical target selection by thalamic axons. Science, 281, 559–62.
Catalano, S. M. , Robertson, R. T ., & Killackey, H. P . (1991). Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proceedings of the National Academy of Sciences of the U S A, 88, 2999–3003.
Charnay, Y. , Paulin, C. , Dray, F. , et al. (1984). Distribution of enkephalin in human fetus and infant spinal cord: an immunofluorescence study. Journal of Comparative Neurology, 223, 415–23.
Coggeshall, R. E. , Jennings, E. A ., & Fitzgerald, M . (1996). Evidence that large myelinated primary afferent fibers make synaptic contacts in lamina II of neonatal rats. Brain Research Developmental Brain Research, 92, 81–90.
Cook, C. J. , Gluckman, P. D. , Johnston, B. M. , et al. (1987). The development of the somatosensory evoked potential in the unanaesthetized fetal sheep. Journal of Developmental Physiology, 9, 441–55.
Craig, K. D. , Whitfield, M. F. , Grunau, R. V. , et al. (1993). Pain in the preterm neonate: behavioural and physiological indices [published erratum appears in Pain 1993, 54, 111]. Pain, 52, 287–99.
Crossley, K. J. , Nicol, M. B. , Hirst, J. J. , et al. (1997). Suppression of arousal by progesterone in fetal sheep. Reproduction, Fertility and Development, 9, 767–73.
Crossley, K. J. , Walker, D. W. , Beart, P. M. , et al. (2000). Characterisation of GABA(A) receptors in fetal, neonatal and adult ovine brain: region and age related changes and the effects of allopregnanolone. Neuropharmacology, 39, 1514–22.
Crowley, J. C. & Katz, L. C. (2000). Early development of ocular dominance columns Science, 290, 1271–3.
de Vries, J. I . & Fong, B. F . (2006). Normal fetal motility: and overview. Ultrasound in Obstetrics and Gynecology, 27, 701–11.
de Vries, J. I. , Visser, G. H. , & Prechtl, H. F. (1982). The emergence of fetal behaviour. I. Qualitative aspects. Early Human Development, 7, 301–22.
Ekholm, J . (1967). Postnatal changes in cutaneous reflexes and in the discharge pattern of cutaneous and articular sense organs. A morphological and physiological study in the cat. Acta Physiologica Scandinavica Supplementum, 297, 1–130.
Erberich, S. G. , Panigraphy, A. , Friedlich, P. , et al. (2006). Somatosensory lateralization in the newborn brain. NeuroImage, 29, 155–61.
Fitzgerald, M . & Koltzenburg, M . (1986). The functional development of descending inhibitory pathways in the dorsolateral funiculus of the newborn rat spinal cord. Brain Research, 389, 261–70.
Fitzgerald, M . (1987a). Prenatal growth of fine-diameter primary afferents into the rat spinal cord: a transganglionic tracer study. Journal of Comparative Neurology, 261, 98–104.
Fitzgerald, M . (1987b). Spontaneous and evoked activity of fetal primary afferents in vivo. Nature, 326, 603–5.
Fitzgerald, M . (1991). A physiological study of the prenatal development of cutaneous sensory inputs to dorsal horn cells in the rat. Journal of Physiology, 432, 473–82.
Fitzgerald, M. , Butcher, T ., & Shortland, P . (1994). Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn. Journal of Comparative Neurology, 348, 225–33.
Fitzgerald, M. , Reynolds, M. L ., & Benowitz, L. I . (1991). GAP-43 expression in the developing rat lumbar spinal cord. Neuroscience, 41, 187–99.
Ghosh, A . & Shatz, C. J . (1992). Involvement of subplate neurons in the formation of ocular dominance columns. Science, 255, 1441–3.
Giordano, J . (1997). Antinociceptive effects of intrathecally administered 2-methylserotonin in developing rats. Brain Research Developmental Brain Research, 98, 142–4.
Goodman, C. S . & Shatz, C. J . (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell, 72, 77–98.
Hepper, P. G. , McCartney, G. R ., & Shannon, E. A . (1998). Lateralised behaviour in first trimester human foetuses. Neuropsychologia, 36, 531–4.
Hjerling-Leffler, J. , AlQatari, M. , Ernfors, P. , et al. (2007). Emergence of functional sensory subtypes as defined by transient receptor potential channel expression. Journal of Neuroscience, 27, 2435–43.
Hogg, I. D . (1941). Sensory nerves and associated structures in the skin of human fetuses of 8 to 14 weeks of menstrual age correlated with functional capacity. Journal of Comparative Neurology, 75, 371–410.
Huang, J. J. , Zhang, X. M ., & McNaughton, P. A . (2006). Modulation of temperature-sensitive TRP channels. Seminars in Cell and Developmental Biology, 17, 638–45.
Humphrey, T . (1978). Function of the nervous system during prenatal life. In Perinatal Physiology, eds. U. Stave & A. A. Weech . New York: Plenum Press, pp. 651–83.
Inan, M. , Lu, H. C. , Albright, M. J. , et al. (2006). Barrel map development relies on protein kinase A regulatory subunit II beta-mediated cAMP signalling. Journal of Neuroscience, 26, 4338–49.
Jennings, E . & Fitzgerald, M . (1996). C-fos can be induced in the neonatal rat spinal cord by both noxious and innocuous peripheral stimulation. Pain, 68, 301–6.
Jennings, E . & Fitzgerald, M . (1998). Postnatal changes in responses of rat dorsal horn cells to afferent stimulation: a fibre-induced sensitization. Journal of Physiology, 509, 859–68.
Jessell, T. M. , Yoshioka, K ., & Jahr, C. E . (1986). Amino acid receptor-mediated transmission at primary afferent synapses in rat spinal cord. Journal of Experimental Biology, 124, 239–58.
Kanold, P. O . & Shatz, C. J . (2006). Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron, 51, 627–38.
Klimach, V. J . & Cooke, R. W . (1988). Maturation of the neonatal somatosensory evoked response in preterm infants. Developmental Medicine and Child Neurology, 30, 208–14.
Kozuma, S. , Okai, T. , Nemoto, A. , et al. (1997). Developmental sequence of human fetal body movements in the second half of pregnancy. American Journal of Perinatology, 14, 165–9.
Leamey, C. A . & Ho, S. M . (1998). Afferent arrival and onset of functional activity in the trigeminothalamic pathway of the rat. Brain Research Developmental Brain Research, 105, 195–207.
Leamey, C. A. , Flett, D. L. , Ho, S. M. , et al. (2007). Development of structural and functional connectivity in the thalamocortical somatosensory pathway in the wallaby. European Journal of Neuroscience, 25, 3058–70.
LeVay, S. , Stryker, M. P ., & Shatz, C. J . (1978). Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study. Journal of Comparative Neurology, 179, 223–44.
Lloyd-Thomas, A. R . & Fitzgerald, M . (1996). Do fetuses feel pain? Reflex responses do not necessarily signify pain. British Medical Journal, 313, 797–8.
Mallat, M. , Houlgatte, R. , Brachet, P. , et al. (1989). Lipopolysaccharide-stimulated rat brain macrophages release NGF in vitro. Developmental Biology, 133, 309–11.
Marmigère, F . & Ernfors, P . (2007). Specification and connectivity of neuronal subtypes in the sensory lineage. Nature, 8, 114–27.
Marti, E. , Gibson, S. J. , Polak, J. M. , et al. (1987). Ontogeny of peptide- and amine-containing neurones in motor, sensory, and autonomic regions of rat and human spinal cord, dorsal root ganglia, and rat skin. Journal of Comparative Neurology, 266, 332–59.
McIntyre, A. K. , Proske, U ., & Rawson, J. A . (1989). Corticofugal action on transmission of group I input from the hindlimb to the pericruciate cortex in the cat. Journal of Physiology, 416, 19–30.
Mirnics, K . & Koerber, H. R . (1995). Prenatal development of rat primary afferent fibers: II. Central projections. Journal of Comparative Neurology, 355, 601–14.
Molnar, Z . & Blakemore, C . (1995). How do thalamic axons find their way to the cortex? Trends in Neurosciences, 18, 389–97.
Molnar, Z. , Lopez-Bendito, G. , Small, J. , et al. (2002). Normal development of embryonic thalamocortical connectivity in the absence of evoked synaptic activity. Journal of Neuroscience, 22, 10313–23.
Nandi, R . & Fitzgerald, M . (2005). Opioid analgesia in the newborn. European Journal of Pain, 9, 105–8.
Narayanan, C. H. , Fox, M. W ., & Hamburger, V . (1971). Prenatal development of spontaneous and evoked activity in the rat (Rattus norvegicus albinus). Behaviour, 40, 100–34.
Nicol, M. B. , Hirst, J. J ., & Walker, D. W . (1998). Effect of pregnane steroids on electrocortical activity and somatosensory evoked potentials in fetal sheep. Neuroscience Letters, 253, 111–14.
Okado, N . (1981). Onset of synapse formation in the human spinal cord. Journal of Comparative Neurology, 201, 211–19.
Pearce, A. R . & Marotte, L. R . (2003). The first thalamocortical synapses are made in the cortical plate in the developing visual cortex of the wallaby (Macropus eugenii). Journal of Comparative Neurology, 461, 205–16.
Penn, A. A . & Shatz, C. J . (1999). Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatric Research, 45, 447–58.
Price, D. J. , Kennedy, H. , Dehay, C. , et al. (2006). The development of cortical connections. European Journal of Neuroscience, 23, 910–20.
Rahman, W. , Dashwood, M. R. , Fitzgerald, M. , et al. (1998). Postnatal development of multiple opioid receptors in the spinal cord and development of spinal morphine analgesia. Brain Research Developmental Brain Research, 108, 239–54.
Rees, S. , Nitsos, I ., & Rawson, J . (1994a). The development of cutaneous afferent pathways in fetal sheep: a structural and functional study. Brain Research, 661, 207–22.
Rees, S. , Rawson, J. , Nitsos, I. , et al. (1994b). The structural and functional development of muscle spindles and their connections in fetal sheep. Brain Research, 642, 185–98.
Schlaggar, B. L . & O'Leary, D. D . (1991). Potential of visual cortex to develop an array of functional units unique to somatosensory cortex. Science, 252, 1556–60.
Schouenborg, J. (2008). Action-based sensory encoding in spinal sensorimotor circuits. Brain Research Reviews, 57, 111–17.
Slater, R. , Cantarella, A. , Gallella, S. , et al. (2006). Cortical pain responses in human infants. Journal of Neuroscience, 26, 3662–6.
Spitzer, N. C . (1994). Spontaneous Ca2+ spikes and waves in embryonic neurons: signaling systems for differentiation. Trends in Neurosciences, 17, 115–18.
Terenghi, G. , Sundaresan, M. , Moscoso, G. , et al. (1993). Neuropeptides and a neuronal marker in cutaneous innervation during human foetal development. Journal of Comparative Neurology, 328, 595–603.
Ververs, I. A. , de Vries, J. I. , van Geijn, H. P. , et al. (1994). Prenatal head position from 12–38 weeks. II. The effects of fetal orientation and placental localization. Early Human Development, 39, 93–100.
Weber, E. D . & Stelzner, D. J . (1977). Behavioral effects of spinal cord transection in the developing rat. Brain Research, 125, 241–55.
Willis, W. D . & Coggeshall, R. E . (2004). Sensory Mechanisms of the Spinal Cord. New York: Plenum Press.