Effects of neonatal transection of the infraorbital nerve upon the structural and functional organization of the ventral posteromedial nucleus in the rat
Nicolas L. Chiaia
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorWilliam R. Bauer
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorShujie Zhang
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorTod A. King
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorPaul C. Wright
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorScott C. Hobler
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorKeith A. Freeman
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorNicolas L. Chiaia
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorWilliam R. Bauer
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorShujie Zhang
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorTod A. King
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorPaul C. Wright
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorScott C. Hobler
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorKeith A. Freeman
Department of Anatomy, Medical College of Ohio, Toledo, Ohio 43699
Search for more papers by this authorAbstract
The present study examined the way in which an indirect partial deafferentation of the medial portion of the ventrobasal complex (VPM/VPL) induced by neonatal transection of the infraorbital nerve (ION) altered the structural and functional properties of its constituent neurons. This manipulation significantly reduced the volume of the contralateral VPM/VPL. In addition, cell counts in Nissl-stained material revealed a significant reduction of the number of VPM/VPL neurons contralateral to neonatal ION transection. We also analyzed the effect of neonatal ION transection on the soma-dendritic morphology of individual neurons in the ventral posteromedial nucleus of the thalamus (VPM) by intracellular injection of horseradish peroxidase (HRP) in vivo and Lucifer yellow in fixed slices. Neonatal transection of the ION resulted in increased dendritic length, area, and volume of VPM neurons in both preparations; however only the changes observed in fixed slices reached statistical significance. Alterations in the functional characteristics of VPM neurons were also observed following neonatal nerve damage. There was a significant decrease in the percentage of vibrissae-sensitive neurons and a corresponding increase in the percentages of neurons responsive to guard hair deflection or that were unresponsive to peripheral stimulation. Neonatal nerve damage also resulted in significantly longer latencies of VPM cells after stimulation of either trigeminal nucleus principalis or subnucleus interpolaris.
The present results indicate that the development of normal response properties and soma-dendritic morphology of VPM neurons is dependent upon intact afferent input during development. Indirect partial deafferentation of VPM/VPL by neonatal transection of the ION results in reduced neuron number, which may result in decreased competition among the dendrites of these neurons. This proposal is consistent with observations of increased dendritic dimensions of VPM neurons contralateral to neonatal ION damage. © 1992 Wiley-Liss, Inc.
Literature Cited
- Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29: 775.
- Akhtar, N. D., and P. W. Land (1991) Activity-dependent regulation of glutamic acid decarboxylase in the rat barrel cortex: Effects of neonatal versus adult sensory deprivation. J. Comp. Neurol. 307: 200–213.
- Armstrong-James, M., and C. A. Callahan (1991) Thalamo-cortical processing of vibrissal information in the rat. 2. Spatiotemporal convergence in the thalamic ventroposterior medial nucleus (VPM) and its relevance to generation of receptive fields of SI cortical barrel neurones. J. Comp. Neurol. 303: 211–224.
- Belford, G. R., and H. P. Killackey (1979a) Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J. Comp. Neurol. 183: 305–322.
- Belford, G. R., and H. P. Killackey (1979b) The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat. J. Comp. Neurol. 188: 63–74.
- Chiaia, N. L., R. W. Rhoades, C. A. Bennett-Clarke, S. E. Fish, and H. P. Killackey (1991a) Thalamic processing of vibrissal information in the rat. I. Afferent input to the medial ventral posterior and posterior nuclei. J. Comp. Neurol. 314: 201–216.
- Chiaia, N. L., R. W. Rhoades, S. E. Fish, and H. P. Killackey (1991b) Thalamic processing of vibrissal information in the rat. II. Morphological and functional properties of medial ventral posterior nucleus and posterior nucleus neurons. J. Comp. Neural. 314: 217–236.
- Chiaia, N. L., P. R. Hess, and R. W. Rhoades (1987) Preventing regeneration of infraorbital axons does not alter the ganglionic or transganglionic consequences of neonatal transection of this trigeminal branch. Dev. Brain Res. 36: 75–88.
- Cullen, M. J., and I. R. Kaiserman-Abramof (1976) Cytological organization of the dorsal lateral geniculate nuclei in mutant anophthalmic and postnatally enucleated mice. J. Neurocytol. 5: 407–424.
- Durham, D., and T. A. Woolsey (1984) Effects of neonatal whisker lesions on mouse central trigeminal pathways. J. Comp. Neurol. 223: 424–447.
- Erzurumlu, R. S., and F. F. Ebner (1986) The effect of neonatal trigeminal nerve lesions on the lemniscal terminals in mouse “barreloids.” Soc. Neurosci. Absts. 12: 126.
- Eysel, U., L. Peichl, and H. Wässle (1985) Dendritic plasticity in the early postnatal feline retina: Quantitative characteristics and sensitive period. J. Comp. Neurol. 242: 134–145.
-
Hamori, J.,
C. Savy,
M. Madarasz,
J. Somogyi,
J. Takacs,
R. Verley, and
E. Farkas-Bargeton
(1986)
Morphological alterations in subcortical vibrissal relays following vibrissal follicle destruction at birth in the mouse.
J. Comp. Neurol.
254:
166–183.
10.1002/cne.902540203 Google Scholar
- Hamori, J., J. Takacs, R. Verley, P. Petrusz, and E. Farkas-Bargeton (1990) Plasticity of GABA-and glutamate-containing terminals in the mouse thalamic ventrobasal complex deprived of vibrissal afferents: An immunogold-electron microscopic study. J. Comp. Neurol. 302: 739–748.
- Harris, R. M. (1986) Morphology of physiologically identified thalamocortical relay neurons in the rat ventrobasal thalamus. J. Comp. Neurol. 251: 491–505.
- Harris, R. M., and T. A. Woolsey (1979) Morphology of Golgi-impregnated neurons in mouse cortical barrels following vibrissae damage at different postnatal ages. Brain Res. 161: 143–149.
- Henderson, T. A., P. D. Kaszubski, J. A. Yelon, and M. F. Jacquin (1988) Effects of neonatal infraorbital nerve section on trigeminal brainstem cell number and dendritic orientation. Soc. Neurosci. Absts. 14: 474.
- Heumann, D., and T. Rabinowicz (1980) Postnatal development of the dorsal lateral geniculate nucleus in the normal and enucleated albino mouse. Exp. Brain Res. 38: 75–85.
- Jacquin, M. F. (1989) Structure-function relationships in the rat brainstem subnucleus interpolaris. V. Functional consequences of neonatal infraorbital nerve transection. J. Comp. Neur. 282: 63–79.
- Jacquin, M. F., R. D. Mooney, and R. W. Rhoades (1986) Morphology, response properties, and collateral projections of trigeminothalamic neurons in brainstem subnucleus interpolaris of rat. Exp. Brain Res. 61: 457–468.
-
Kanosue, K.,
T. Nakayama,
P. D. Andrew,
Z. Shen, and
M. Sato
(1986)
Neuronal activities in ventrobasal complex of thalamus and in trigeminal main sensory nucleus during EEG desynchronization in anesthetized rats.
Brain Res.
379:
90–97.
10.1016/0006-8993(86)90259-3 Google Scholar
- Killackey, H. P., and G. R. Belford (1979) The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J. Comp. Neurol. 183: 285–304.
- Killackey, H. P., and K. Fleming (1985) The role of the principal sensory nucleus in central trigeminal pattern formation. Dev. Brain Res. 22: 141–145.
- Killackey, H. P., G. O. Ivy, and T. J. Cunningham (1978) Anomalous organization of SmI somatotopic map consequent to vibrissae removal in the newborn rat. Brain Res. 155: 136–140.
- Killackey, H. P., and S. Leshin (1975) The organization of specific thalamocortical projections to the posteromedial barrel subfield of the rat somatic sensory cortex. Brain Res. 86: 469–472.
- Killackey, H. P., and A. Shinder (1981) Central correlates of peripheral pattern alterations in the trigeminal system of the rat. II. The effect of nerve section. Dev. Brain Res. 1: 121–126.
- Kirby, M. A., and L. M. Chalupa (1986) Retinal crowding alters the morphology of alpha ganglion cells. J. Comp. Neurol. 251: 532–541.
-
Land, P. W., and
D. J. Simons
(1985)
Metabolic activity in SmI cortical barrels of adult rats is dependent on patterned sensory stimulation of the mystacial vibrissae.
Brain Res.
341:
189–194.
10.1016/0006-8993(85)91488-X Google Scholar
- Leventhal, A. G., J. D. Schall, and S. J. Ault (1988) Extrinsic determinants of retinal ganglion cell structure in the cat. J. Neurosci. 8: 2028–2038.
- Ma, P. M. (1991) The barrelettes-architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. I. Normal structural organization. J. Comp. Neurol. 309: 161–199.
- Ma, P. M., and T. A. Woolsey (1984) Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. Brain Res. 306: 374–379.
- Nicolelis, M. A. L., J. K. Chapin, and R. C. S. Lin (1991) Thalamic plasticity induced by early whisker removal in rats. Brain Res. 561: 344–349.
- Oh, L. J., G. Kim, J. Yu, and R. T. Robertson (1991) Transneuronal degeneration of thalamic neurons following deafferentation: quantitative studies using [3H]thymidine autoradiography. Brain Res. 63: 191–200.
- Perry, V. H., and R. Linden (1982) Evidence for dendritic competition in the developing retina. Nature 297: 683.
- Perry, V. H., and L. Maffei (1988) Dendritic competition: Competition for what? Dev. Brain Res. 41: 195–208.
- Peschanski, M., C. L. Lee, and R. J. Ralston III (1984) The structural organization of the ventrobasal complex of the rat as revealed by the analysis of physiologically characterized neurons injected intracellularly with horseradish peroxidase. Brain Res. 279: 63–74.
- Rakic, P. (1975) Role of cell interaction in development of dendritic patterns. Adv. Neurol. 12: 117–134.
- Rhoades, R. W., S. E. Fish, R. D. Mooney, and N. L. Chiaia (1987) Distribution of visual callosal projection neurons in hamsters subjected to transection of the optic radiations on the day of birth. Dev. Brain Res. 32: 217–232.
- Rubel, E. W., R. L. Hyson, and D. Durham (1990) Afferent regulation of neurons in the brain stem auditory system. J. Neurobiol. 21: 169–196.
- Saporta, S., and L. Kruger (1977) The organization of thalamocortical relay neurons in the rat ventrobasal complex studied by the retrograde transport of horseradish Peroxidase 174: 187–208.
- Shosaku, A. (1985) A comparison of receptive field properties of vibrissa neurons between the rat thalamic reticular and ventro-basal nuclei. Brain Res. 347: 36–40.
- Sholl, D. A. (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87: 387–401.
- Simons, D. J., and G. E. Carvell (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J. Neurophysiol. 61: 311–330.
- Simons, D. J., D. Durham, and T. A. Woolsey (1984) Functional organization of mouse and rat SmI barrel cortex following vibrissal damage on different postnatal days. Somatosens. Res. 1: 207–245.
- Smolen, A. J., Wright, and R. J. Cunningham (1983) Neuron numbers in the superior cervical sympathetic ganglion of the rat: A critical comparison of methods for cell counting. J. Neurocytol. 12: 739–750.
- Steffen, M., and H. Van der Loos (1980) Early lesions of mouse vibrissal follicles; their influence on dendrite orientation in the cortical barrelfield. Exp. Brain Res. 40: 419–431.
- Sugita, S., and K. Otani (1983) Quantitative analysis of the lateral geniculate nucleus in the mutant microphthalmic rat. Exp. Neurol. 82: 413–423.
-
Sugita, S.,
K. Otani, and
G. Kato
(1986)
Neurons of the dorsal lateral geniculate nucleus of the hereditary microphthalmic rat: A Golgi study.
Neurosci. Res.
3:
384–394.
10.1016/0168-0102(86)90030-1 Google Scholar
- Sumitomo, I., and K. Iwama (1987) Neuronal organization of rat thalamus for processing information of vibrissal movements. Brain Res. 415: 389–392.
- Van der Loos, H. (1976) Barreloids in mouse somatosensory thalamus. Neurosci. Lett. 2: 1–6.
- Van der Loos, H., and T. A. Woolsey (1973) Somatosensory cortex: Structural alterations following early injury to sense organs. Science 179: 395–398.
-
Verley, R., and
I. Onnen
(1981)
Somatotopic organization of the tactile thalamus in normal adult and developing mice and in adult mice dewhiskered since birth.
Exp. Neurol.
72:
462–474.
10.1016/0014-4886(81)90236-3 Google Scholar
- Waite, P. M. E. (1973) Somatotopic organization of vibrissal responses in the ventrobasal complex of the rat thalamus. J. Physiol. (Lond.) 228: 527–540.
- Waite, P. M. E. (1984) Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section. J. Physiol. (Lond.) 352: 425–445.
- Waite, P. M. E., and B. G. Cragg (1982) The peripheral and central changes resulting from cutting or crushing the afferent nerve supply to the whiskers. Proc. R. Soc. Lond. [Biol.] 214: 191–211.
- Waite, P. M. E., and P. K. Taylor (1978) Removal of whiskers in young rats causes functional changes in cerebral cortex. Nature 274: 600–602.
- Woolsey, T., and H. Van der Loos (1970) The structural organization of Layer IV in the somatosensory region (SI) of mouse cerebral cortex: The description of a cortical fieldcomposed of discreet cytoarchitectonic units. Brain Res. 17: 205–242.
- Woolsey, T. A., J. R. Anderson, J. R. Wann, and B. B. Stanfield (1979) Effects of early vibrissae damage on neurons in the ventrobasal (VB) thalamus of the mouse. J. Comp. Neurol. 184: 363–380.
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