- Email: [email protected]
Transganglionic degeneration in the spinal trigeminal nucleus following removal of tooth pulps in adult cats
Brain Research, 101 (1976) 137-140 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
137
Short Communications
Transganglionic degeneration in the spinal trigeminal nucleus following removal of tooth pulps in adult cats*
LESN1CK E. WESTRUM, ROBERT C. CANFIELD AND RICHARD G. BLACK Departments of Neurological Surgery, Biological Structure, Restorative Dentistry and Anesthesiology, University of Washington, Seattle, Wash. 98195 (U.S.A.)
(Accepted September 15th, 1975)
It is generally thought that transganglionic degeneration of central axons following lesions of their peripheral processes does not occur in adult nervous systemS, 6. For this reason there has been a lack of anatomical descriptions of the central distribution of specific groups of peripheral sensory axons. We, however, have found reproducible axonal and terminal degeneration in specific regions of the spinal trigeminal nucleus in adult cats following tooth pulpectomies 12. Healthy adult cats were used and the absence of dental pathology was confirmed prior to operation and in the controls. Under pentobarbital anesthesia and using appropriate aseptic dental procedures, the pulps were completely removed from all of the teeth on one side of 12 animals. Following postoperative survival times of 7, 9, 11, 14, 21, 28 and 100 days the animals were perfused with 4~o formaldehyde in a phosphate buffer 11. Transverse frozen sections through the brain stem, including the major parts of the spinal trigeminal nucleus, were stained by either the N a u t a Gygax v or the Fink-Heimer (I) 4 technique. Two normal, unoperated animals were sacrificed and processed in the same fashion to serve as controls. Fig. 1 illustrates the pattern of degeneration observed at 1 l days. Unequivocal axonal and terminal degeneration (Fig. 2) is seen predominantly in the ventral half to one-third of the subnucleus interpolaris of the spinal trigeminal complex, near and immediately rostral to the obex, with very much less in the adjacent subnuclei (caudalis and oralis). The distribution is bilateral, but heaviest on the side of the lesion. The occurrence of contralateral degeneration is surprising in view of what is known of the organization of this system 2, but it is a consistent finding here. A crossing pathway of degenerating fibers cannot be identified with certainty. The amount of degeneration is less at shorter or longer survivals, but the pattern is similar in each. Control animals, with healthy teeth, show no degeneration. * Correspondence and reprint requests should be sent to Dr. L. E. Westrum, Department of Neurological Surgery, University of Washington, RI-20, Seattle, Wash. 98195, U.S.A.
138 1.. -2.0
0.5
2.0
4.0
Fig. 1. A drawing of silver-stained sections from an animal surviving ! 1 days after complete unilateral tooth pulpectomies, to show the degeneration pattern in the various subnuclei of the spinal trigeminal complex. The two middle sections are from pars interpolaris, the upper from rostral pars caudalis and the lower from pars oralis. The numbers to the left represent the approximate distances in mm from the obex. The unoperated side is marked with an R. Irregular, wavy lines represent degenerating axons and dots represent degenerating terminals. The results demonstrate a definite sequence and reproducible pattern of axonal and terminal degeneration associated with tooth pulp removal and suggest an anatomically definable area of representation for tooth pulps in the spinal trigeminal nucleus. The area corresponds well with the distribution of tooth pulp afferents found in some electrophysiological studiesZ, s and possibly with an anatomical cell group described for this same subnucleus t°. I f the chromatolysis of ganglion cells, following dental surgery 1,9,1~, does lead to degeneration of the central axonal processes 6 this would account for the observations in the present paper. Although 'transganglionic sensory degeneration' has been associated with immature rather than mature nervous systems5, 6, the studies of such ganglion cell changes have not usually been accompanied by parallel or subsequent investigations of the appropriate regions in the central nervous system. Although the results may indicate a peculiarity of the trigeminal system, it may be that more careful studies will reveal this to be a more common phenomenon than has hitherto been thought. Since some of the anatomical work suggests recovery of ganglion cells after dental surgery 9, the degeneration of the central processes and terminals may be a transient event followed by recovery, sprouting or regeneration 6. Obviously, a careful
139
Fig. 2. A view of the ventral one-half of pars interpolaris on the side of the pulpectomies to show the character and density of degeneration at 11 days survival. D is dorsal and T is part of the spinal trigeminal tract with a few degenerating fibers nearby. Fink-Heimer stain. × 200.
study o f the cells in b o t h ganglia, f r o m the o p e r a t e d p r e p a r a t i o n s described here, a n d an electron m i c r o s c o p i c study o f the d e g e n e r a t i n g central axonal processes a n d terminals are required. This w o r k was s u p p o r t e d by N a t i o n a l Institutes o f H e a l t h Research G r a n t s N S 09678 a n d N S 04053 a w a r d e d by the N a t i o n a l Institute o f N e u r o l o g i c a l a n d C o m m u n i c a t i v e Disorders a n d Stroke, P H S / D H E W and G r a n t 11.0220 from the University of Washington. The a u t h o r s gratefully a c k n o w l e d g e this s u p p o r t and wish to t h a n k Jerry M a d docks, V l a d i m i r Uhlir, S t u a r t W a t e r m a n a n d Z o l t a n Z e l e n a k for technical assistance a n d A n n H a r r i s for secretarial help. The a u t h o r s also t h a n k Dr. A. R. L i e b e r m a n for helpful suggestions.
1 BRASHEAR,A. D., The innervation of the teeth, J. comp. Neurol., 64 (1936) 169-185. 2 DARIAN-SMITH, I., The trigeminal system. In A. IGGO (Ed.), Somatosensory System, Vol. 11, Handbook of Sensory Physiology, Springer, Berlin, 1973, pp. 271-314. 3 DUNKER,E., GRUBEL,G., UND YONRtHREN, D., Dynamische Eigenschaften afferenter Trigeminusneuren in der Medalla oblongata bei electrischer Zahnieizung, Pfliigers Arch. ges. Physiol., 296 (1967) 289-307. 4 FINK, R. P., AND HEXMER,L., Two methods for selective impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374.
140 5 GI',ANT, G., Neuronal changes central to the site ofaxonal transection. A method for identii~cation of retrograde changes in perikarya, dendrites and axons by silver-impregnation. In W..!. t4. NAUTA AND S. O, E. EBBESSON (Eds.), Cr)tltemporarl' Research Metho~t~ iJt ~lem'oamltom~.. Springer, New York, 1970, pp. 173 185. 6 LIEBEa~IA54,A. R., Sensory ganglia. In 1). N. LANDON (Ed.), The Peripheral Nerve, Chapman and Hall, London, 1976, pp. 187-278. 7 NAUrA, W. J. H., ANt) GV(~AX, P. A., Silver impregnation cf degenerating axons in the central nervous system: a modified technic, Stai~r Technol., 29 (195<) 91-93. 8 NORD, S. G., AND YOt;N~_;, R. F'., Projection of tooth pulp alferents to the cat trigeminal nucleus caudalis, Bra#~ Research, 90 (1975) 195-204. 9 STRASSBURG, M., Morphologic reaction of the trigeminal ganglion after experimental surgery on the maxillodental region, J. Oral Surg., 25 (1967) 107-114. 10 TABOR, E., The cytoarchitecture of the brain stem of the cat. I. Brain stern nuclei of cat, .L crm,p. Neurol., 116 (1961) 27 69. 1 I WESTRUM, L. E., ANt) BLACK, R. G., Fine structural aspects of the synaptic organization of the spinal trigeminal nucleus (pars interpolaris) of the cat, Brain Research, 25 (1971) 265-287. 12 WESTRUM, L. E., CANFtELD, R. C., AND BLACK, R. G., Axonal degeneration patterns in the cat brain stem spinal trigeminal nucleus following tooth pulp removal, Int. Ass. Study Paht 1st World Congr., Session ol~ Trigemhzal 5),stem, Florence, (1975). 13 W~NDLZ, W. F., Experimental proof of the types of neurons that innervate the tooth pulp, J, comp. Neuro/., 43 (1927) 347-356.
137
Short Communications
Transganglionic degeneration in the spinal trigeminal nucleus following removal of tooth pulps in adult cats*
LESN1CK E. WESTRUM, ROBERT C. CANFIELD AND RICHARD G. BLACK Departments of Neurological Surgery, Biological Structure, Restorative Dentistry and Anesthesiology, University of Washington, Seattle, Wash. 98195 (U.S.A.)
(Accepted September 15th, 1975)
It is generally thought that transganglionic degeneration of central axons following lesions of their peripheral processes does not occur in adult nervous systemS, 6. For this reason there has been a lack of anatomical descriptions of the central distribution of specific groups of peripheral sensory axons. We, however, have found reproducible axonal and terminal degeneration in specific regions of the spinal trigeminal nucleus in adult cats following tooth pulpectomies 12. Healthy adult cats were used and the absence of dental pathology was confirmed prior to operation and in the controls. Under pentobarbital anesthesia and using appropriate aseptic dental procedures, the pulps were completely removed from all of the teeth on one side of 12 animals. Following postoperative survival times of 7, 9, 11, 14, 21, 28 and 100 days the animals were perfused with 4~o formaldehyde in a phosphate buffer 11. Transverse frozen sections through the brain stem, including the major parts of the spinal trigeminal nucleus, were stained by either the N a u t a Gygax v or the Fink-Heimer (I) 4 technique. Two normal, unoperated animals were sacrificed and processed in the same fashion to serve as controls. Fig. 1 illustrates the pattern of degeneration observed at 1 l days. Unequivocal axonal and terminal degeneration (Fig. 2) is seen predominantly in the ventral half to one-third of the subnucleus interpolaris of the spinal trigeminal complex, near and immediately rostral to the obex, with very much less in the adjacent subnuclei (caudalis and oralis). The distribution is bilateral, but heaviest on the side of the lesion. The occurrence of contralateral degeneration is surprising in view of what is known of the organization of this system 2, but it is a consistent finding here. A crossing pathway of degenerating fibers cannot be identified with certainty. The amount of degeneration is less at shorter or longer survivals, but the pattern is similar in each. Control animals, with healthy teeth, show no degeneration. * Correspondence and reprint requests should be sent to Dr. L. E. Westrum, Department of Neurological Surgery, University of Washington, RI-20, Seattle, Wash. 98195, U.S.A.
138 1.. -2.0
0.5
2.0
4.0
Fig. 1. A drawing of silver-stained sections from an animal surviving ! 1 days after complete unilateral tooth pulpectomies, to show the degeneration pattern in the various subnuclei of the spinal trigeminal complex. The two middle sections are from pars interpolaris, the upper from rostral pars caudalis and the lower from pars oralis. The numbers to the left represent the approximate distances in mm from the obex. The unoperated side is marked with an R. Irregular, wavy lines represent degenerating axons and dots represent degenerating terminals. The results demonstrate a definite sequence and reproducible pattern of axonal and terminal degeneration associated with tooth pulp removal and suggest an anatomically definable area of representation for tooth pulps in the spinal trigeminal nucleus. The area corresponds well with the distribution of tooth pulp afferents found in some electrophysiological studiesZ, s and possibly with an anatomical cell group described for this same subnucleus t°. I f the chromatolysis of ganglion cells, following dental surgery 1,9,1~, does lead to degeneration of the central axonal processes 6 this would account for the observations in the present paper. Although 'transganglionic sensory degeneration' has been associated with immature rather than mature nervous systems5, 6, the studies of such ganglion cell changes have not usually been accompanied by parallel or subsequent investigations of the appropriate regions in the central nervous system. Although the results may indicate a peculiarity of the trigeminal system, it may be that more careful studies will reveal this to be a more common phenomenon than has hitherto been thought. Since some of the anatomical work suggests recovery of ganglion cells after dental surgery 9, the degeneration of the central processes and terminals may be a transient event followed by recovery, sprouting or regeneration 6. Obviously, a careful
139
Fig. 2. A view of the ventral one-half of pars interpolaris on the side of the pulpectomies to show the character and density of degeneration at 11 days survival. D is dorsal and T is part of the spinal trigeminal tract with a few degenerating fibers nearby. Fink-Heimer stain. × 200.
study o f the cells in b o t h ganglia, f r o m the o p e r a t e d p r e p a r a t i o n s described here, a n d an electron m i c r o s c o p i c study o f the d e g e n e r a t i n g central axonal processes a n d terminals are required. This w o r k was s u p p o r t e d by N a t i o n a l Institutes o f H e a l t h Research G r a n t s N S 09678 a n d N S 04053 a w a r d e d by the N a t i o n a l Institute o f N e u r o l o g i c a l a n d C o m m u n i c a t i v e Disorders a n d Stroke, P H S / D H E W and G r a n t 11.0220 from the University of Washington. The a u t h o r s gratefully a c k n o w l e d g e this s u p p o r t and wish to t h a n k Jerry M a d docks, V l a d i m i r Uhlir, S t u a r t W a t e r m a n a n d Z o l t a n Z e l e n a k for technical assistance a n d A n n H a r r i s for secretarial help. The a u t h o r s also t h a n k Dr. A. R. L i e b e r m a n for helpful suggestions.
1 BRASHEAR,A. D., The innervation of the teeth, J. comp. Neurol., 64 (1936) 169-185. 2 DARIAN-SMITH, I., The trigeminal system. In A. IGGO (Ed.), Somatosensory System, Vol. 11, Handbook of Sensory Physiology, Springer, Berlin, 1973, pp. 271-314. 3 DUNKER,E., GRUBEL,G., UND YONRtHREN, D., Dynamische Eigenschaften afferenter Trigeminusneuren in der Medalla oblongata bei electrischer Zahnieizung, Pfliigers Arch. ges. Physiol., 296 (1967) 289-307. 4 FINK, R. P., AND HEXMER,L., Two methods for selective impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Research, 4 (1967) 369-374.
140 5 GI',ANT, G., Neuronal changes central to the site ofaxonal transection. A method for identii~cation of retrograde changes in perikarya, dendrites and axons by silver-impregnation. In W..!. t4. NAUTA AND S. O, E. EBBESSON (Eds.), Cr)tltemporarl' Research Metho~t~ iJt ~lem'oamltom~.. Springer, New York, 1970, pp. 173 185. 6 LIEBEa~IA54,A. R., Sensory ganglia. In 1). N. LANDON (Ed.), The Peripheral Nerve, Chapman and Hall, London, 1976, pp. 187-278. 7 NAUrA, W. J. H., ANt) GV(~AX, P. A., Silver impregnation cf degenerating axons in the central nervous system: a modified technic, Stai~r Technol., 29 (195<) 91-93. 8 NORD, S. G., AND YOt;N~_;, R. F'., Projection of tooth pulp alferents to the cat trigeminal nucleus caudalis, Bra#~ Research, 90 (1975) 195-204. 9 STRASSBURG, M., Morphologic reaction of the trigeminal ganglion after experimental surgery on the maxillodental region, J. Oral Surg., 25 (1967) 107-114. 10 TABOR, E., The cytoarchitecture of the brain stem of the cat. I. Brain stern nuclei of cat, .L crm,p. Neurol., 116 (1961) 27 69. 1 I WESTRUM, L. E., ANt) BLACK, R. G., Fine structural aspects of the synaptic organization of the spinal trigeminal nucleus (pars interpolaris) of the cat, Brain Research, 25 (1971) 265-287. 12 WESTRUM, L. E., CANFtELD, R. C., AND BLACK, R. G., Axonal degeneration patterns in the cat brain stem spinal trigeminal nucleus following tooth pulp removal, Int. Ass. Study Paht 1st World Congr., Session ol~ Trigemhzal 5),stem, Florence, (1975). 13 W~NDLZ, W. F., Experimental proof of the types of neurons that innervate the tooth pulp, J, comp. Neuro/., 43 (1927) 347-356.