The role of the principal sensory nucleus in central trigeminal pattern formation

Developmental Brain Research, 22 (1985) 141-145 Elsevier

141

BRD 60087

The role of the principal sensory nucleus in central trigeminal pattern formation HERBERT P. KILLACKEY and KIRK FLEMING

Department of Psychobiology, Universityof California, lrvine, CA 92717 (U.S.A.) (Accepted April 23rd, 1985)

Key words: trigeminal system - - ventral posterior nucleus - - vibrissa - - barrel - - development

Complete lesions of the principal sensory nucleus in the neonatal rat disrupts vibrissae-related pattern formation in the ventral posterior nucleus of the dorsal thalamus. Similar lesions of the spinal trigeminal nucleus do not effect pattern formation in the ventral posterior nucleus. The results are interpreted as suggesting that the principal sensory nucleus provides a template for pattern formation in central trigeminal structures.

At each synaptic level of the rodent trigeminal system between the periphery and the cerebral cortex the distribution of ascending afferent fibers and their target neurons are characterized by a discrete distribution pattern which replicates the pattern of mystacial vibrissae and sinus hairs on the snout4, 7, 12,14,15,18,21. These maps of the sensory surface form in a temporal sequence beginning at the periphery and concluding in the somatosensory cortex 5,9. It has also been demonstrated that early perturbations to the snout, such as removing a row of vibrissae, result in correlated changes in each of the central mapsS,6, 20. In total, these results have been interpreted as suggesting that the periphery plays a role in guiding the formation of central trigeminal patterns 13A9 and that the brainstem serves a particularly important role in this process 2,5,13. However, as discussed below, the brainstem trigeminal complex can be subdivided into a number of component parts and the question of which portion of this complex plays a role in this process has not been directly addressed. The principal components of the rat brainstem trigeminal complex are the principal sensory nucleus and the spinal trigeminal nucleus which is in turn composed of the subnuclei oralis, interpolaris and caudalis 4.17. The available evidence indicates that collaterals of a single trigeminal afferent innervates each of these subdivisions 11. Further, the terminals of

these trigeminal ~fferents form a vibrissae-related pattern in at least 3 of the subdivisions; the principal sensory nucleus, the subnucleus interpolaris and the subnucleus caudalis 4. In turn, at least portions of all 3 of these subdivisions project to the ventral posterior nucleus of the dorsal thalamus. Both the principal sensory nucleus and the subnucleus interpolaris project topographically to the ventral posterior nucleusS, 16 and a portion of the subnucleus caudalis outside the area of vibrissae representation also projects to this nucleus 10. This considerable divergence of the trigeminal pathway at the brainstem level and the subsequent convergence at the level of the thalamus obscures the role of individual brainstem trigeminal nuclei in central trigeminal pattern formation. With this in mind, we decided to investigate the role of the individual subdivisions of the brainstem trigeminal sensory complex on thalamic pattern formation by making selective lesions of the rat brainstem trigeminal complex on the day of birth and assaying the effects of these lesions on pattern formation in the ventral posterior nucleus several days later. In this study 43 litters of neonatal S p r a g u e Dawley rats were employed; because making discrete lesions within the neonatal rat brainstem trigeminal complex proved to be difficult, useful data were obtained from only 17 neonatal rats. On the day of birth, neonatal rats were placed on a bed of shaved

Correspondence: H. P. Killackey, Department of Psychobiology, University of California, Irvine, Irvine, CA 92717, U.S.A. 0165-3806/85/$03.30 © 1985 Elsevier Science Publishers B.V. (Biomedical Division)

142 ice until immobilized and insensitive to tail pinch. The skull was exposed and an electrode was inserted into the brainstem using surface l a n d m a r k s as a guide. Lesions were m a d e by passing 180/~A of current for 10 s. A f t e r surgery, the skin incision was closed and the neonatal rat r e t u r n e d to its mother. A f t e r 6 - 8 days, the animals were sacrificed under ether anesthesia and perfused transcardially with a solution of 10% glycerol/0.5% formalin in distilled water. The brains were r e m o v e d and frozen in isopentane at a t e m p e r a t u r e o f - 4 0 °C. C o r o n a l sections 30 # m thick were cut in a cryostat. The sections were stained for the localization of the mitochondrial enzyme succinic d e h y d r o g e n a s e ( S D H ) by incubation in a 37 °C-solution of sodium succinate and nitro blue tetrazolium in p h o s p h a t e buffer 14. The sections were then counterstained with toluidine blue. Following these procedures, we have found that neither restricted lesions of subnuclei interpolaris or caudalis alone nor large lesions involving both these subnuclei and the descending limb of the trigeminal tract disrupt the formation of a vibrissae-related pattern in the ventral posterior nucleus. H o w e v e r , lesions of the principal sensory nucleus which do not a p p e a r to encroach on the trigeminal tract (it was of normal width and free of gliosis) do disrupt the vibrissae-related pattern in the ventral posterior nucleus. This finding is illustrated in Fig. 1. The top p h o t o m i crographs illustrate the normal (left) and completely destroyed principal sensory nucleus (right) from one animal. The middle photos illustrate the normal pattern of vibrissae-related segmentation in subnucleus interpolaris on both the normal side (left) and the d a m a g e d side (right) of the same animal, d e m o n s t r a ting that in this case interpolaris was not affected by the lesion. A t the bottom, a low-power p h o t o m i c r o graph of a section through the thalamus at the level of the ventral posterior nucleus illustrates the effect of this lesion on this nucleus. On the side contralateral to the lesion (left), the pattern of vibrissae-related segmentation in the affected ventral posterior nucleus is disrupted. In this case, the level of S D H staining within the ventral posterior nucleus is higher than in surrounding thalamic regions. H o w e v e r , within the dorsal portion of the nucleus where the vibrissae representation would normally be, there is no clear relationship between the p a t t e r n of staining and the vibrissae as there is on the normal side (right). A t best,

Fig. 1. The effect that a complete lesion of the principal sensory nucleus on the day of birth has on pattern formation in the ventral posterior nucleus. All photomicrographs are from the same animal which was sacrificed on day 8. Top: on the left is the normal principal sensory nucleus and on the right is the principal sensory nucleus destroyed by a lesion which left intact the trigeminal tract. Middle: the two normally organized subnuclei interpolaris. Bottom: section through the ventral posterior nucleus illustrating the normal vibrissae-related pattern on the right side and the anomalous pattern in the ventral posterior nucleus on the other side (left) which receives projections from the destroyed principal sensory nucleus. See text for further details. Scale bar for the top and middle portion, 0.5 mm; for the bottom portion, 1 mm. the S D H staining is arranged in disorganized clumps. Fig. 2 presents further evidence of this effect. The photomicrographs at the top illustrates the normal principal sensory nucleus (left) and ventral posterior

143

Fig. 2. Pattern formation in the ventral posterior nucleus after complete and partial lesions of the principal sensory nucleus. Each pair of photomicrographs is from the same animal. All animals were sacrificed on day 6. Top: normal pattern of vibrissae representation in the principal sensory nucleus and the ventral posterior nucleus. Middle: principal sensory nucleus completely destroyed by a lesion and a section through the ventral posterior nucleus illustrating the disrupted pattern. Bottom: partial lesion of the caudal portion of the principal sensory nucleus. In this case, dense but aberrant segmentation is still detectable in dorsal and caudal portions of the principal sensory nucleus. At the right is a section through the disorganized portion of the ventral posterior nucleus. See text for further details. Scale bar, 0.5 ram. nucleus (right). Note that in the ventral posterior nucleus the distribution of neurons coincides with the dense patches of S D H staining. The middle photomicrographs illustrate another case, the left photomi-

crograph illustrates the completely destroyed principal sensory nucleus and the right photomicrograph the affected ventral posterior nucleus. In this case, although the density of S D H staining is not particularly high, the distribution of neurons in the ventral portion of the nucleus related to the limbs still correlates with the distribution of S D H 3. However, in the dorsal portion of this nucleus related to the vibrissae it is difficult to make such a correlation. In this portion of the nucleus, the cells are more evenly distributed, although there are some irregular clumps of SDH activity and associated neurons. The bottom portion of Fig. 2 illustrates a case in which the principal sensory nucleus was only partially destroyed. In this case, the lesion was centered on the ventral caudal portion of the principal sensory nucleus and rostral portions of the nucleus appeared relatively intact. However, even in the caudal portion of the principal sensory nucleus areas of dense but unorganized SDH staining could still be detected (left). In this case, the pattern in the ventral posterior nucleus was also disrupted but the effect was localized to only the caudal portion of the nucleus (right). Conversely, partial lesions restricted to the rostral portions of the principal sensory nucleus disrupted the pattern in rostral portions of the ventral posterior nucleus. In interpreting the results of the present experiment it is important to point out that the afferent terminations arising from the principal sensory nucleus are probably a major source of the normal S D H pattern in the ventral posterior nucleus. Hence, some differences in density of staining and pattern after direct damage to the principal sensory nucleus is not unexpected. However, this factor alone cannot account for the current results. Both the anomalous dense staining patterns (bottom of Figs. 1 and 2) and the aberrant distribution of thalamic neurons (middle of Fig. 2) suggest a true change in the organization of the ventral posterior nucleus rather than a simple loss of afferents. In this study, we have demonstrated that the formation of a vibrissae-related pattern in the ventral posterior nucleus is dependent on an intact principal sensory nucleus and not on other portions of the brainstem trigeminal complex. On the basis of this finding, we conclude that during the course of development it is the principal sensory nucleus which plays the major role in transferring peripherally derived in-

144 formation on the distribution of receptors to more central portions of the rat's trigeminal system. Sever-

lamic and cortical trigeminal centers. The present results provide direct support for this hypothesis.

al previous observations support the contention that

The present results also have some bearing on the

it is the principal sensory nucleus which plays the ma-

nature of the topographic relations between the prin-

jor role in pattern formation in more central trigemi-

cipal sensory nucleus of the brainstem and the ventral posterior nucleus. In the present study, partial le-

nal structures. First, the thalamic projections of the principal sensory nucleus are more extensive than

sions of caudal principal sensory nucleus affected

are those of the other subdivisions of the brainstem trigeminal complex8,16. Second, when the thalamic

pattern formation in the caudal ventral posterior nucleus while rostral lesions in the principal sensory nu-

projection neurons of the brainstem trigeminal com-

cleus affected pattern formation in more rostral por-

plex are retrogradely labeled with horseradish perox-

tions of the ventral posterior nucleus. Previous stud-

idase, it is only the thalamic projection n e u r o n s of the principal sensory nucleus which are found to be distributed in a vibrissae-related pattern 7. Further, the

ies have indicated that each vibrissa is represented in the principal sensory nucleus and the ventral posterior nucleus by a cylinder of tissue which extend caudorostrally throughout the respective nuclei 2,~. The present results suggest that a point-to-point relationship between portions of the cylinder representing a single vibrissa is m a i n t a i n e d between the two structures. The functional significance of this relationship is obscure. However, it should be noted that it is this dimension of the topographic organization of central vibrissae representations which is collapsed into the fourth layer of primary somatosensory cortex.

distribution pattern of vibrissae-related thalamic projection cells in the principal sensory nucleus can be altered by neonatal vibrissae damage 1. It has recently been determined that the primary effect of vibrissae damage in the neonatal rat is a deafferentation of the associated portions of the brainstem trigeminal complex 2. The results of this study were interpreted as suggesting that deafferentation results in the failure of the thalamic projection neurons of the principal sensory n e u r o n s to aggregate into a pattern of vibrissae-related clusters and it was hypothesized that the cells of the principal sensory nucleus act as a template for pattern formation in tha-

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This research was supported by National Science Foundation G r a n t BNS 84-18715 to H.P.K.

8 Erzurumlu, R. S. and Killackey, H. P., Diencephalic projections of the subnucleus interpolaris of the brainstem trigeminal complex in the rat, Neuroscience, 5 (1980) 1891-1901. 9 Erzurumlu, R. S. and Killackey, H. P., Development of order in the rat trigeminal system, J. Comp. Neurol., 213 (1983) 365-380. 10 Fukushima, T. and Kerr, F. W. L., Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections, J. Comp. Neurol., 183 (1979) 169-184.

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