Projection of cervical dorsal root fibers to the medulla oblongata in the brush-tailed possum Trichosurus vulpecula.код для вставкиСкачать
THE AMERICAN JOURNAL OF ANATOMY 179:232-242 (1987) Projection of Cervical Dorsal Root Fibers to the Medulla Oblongata in the Brush-Tailed Possum, Trichosurus vulpecula JAMES L. CULBERSON Department of Anatomy, West Virginia University Medical Center, Morgantown, West Virginia 26506 a highly ordered manner, classically described as a layered, dermatotopic' pattern (Ferraro and Barrera, 1935; Kahler, 1882; Kodama, 1942; Kruger and Norton, 1973; Ram6n y Cajal, 1952; Walker and Weaver, 1942). More recently, re-sorting of these fibers into a somatotopic(see footnote 1)arrangement has been recognized (Pubols et al., 1965; Whitsel et al., 1970). Within the DCN, used here to include nucleus gracilis (GN), nucleus cuneatus (CN), and external cuneate nucleus (EC),these fibers are now known to reach particular nuclei, subnuclei, andor areas within subnuclei based on their somatotopic origins (Campbellet al., 1974; Johnson et al., 1968; Kruger et al., 1961)and, to a lesser extent, on their modalities (Blum et al., 1975; Dykes et al., 1982; Millar and Basbaum, 1975; Ostapoff et al., 1983). With the background provided by these studies of somatotopy and modality sorting in several mammalian species, it is possible to examine the distribution of dorsal root fibers to the DCN in any species and to draw limited conclusions about the locations and relative densities of classes of receptors in skin vs. muscle supplied by that particular root. Detailed anatomical descriptions of cervical dorsal root projections to the medulla have been published for the following mammals: rat (Basbaum and Hand, 19731, lesser bushbaby (Albright and Haines, 1978), squirrel (Albright et al., 1983),rhesus monkey (Ferraro and Barrera, 1935; Rustioni et al., 1979; Shiver et al., 1968), and cat (Keller and Hand, 1970; Rustioni and Macchi, 1968). In addition, one previous report (Culberson and Albright, 1984) includes some data on the arrangement of cervical dorsal root fibers in the fasciculus cuneatus of three species-the raccoon, potoroo, and brush-tailed possum; however, details of distribution have not been published for any of these. In the present work, the medullary distribution of cervical dorsal root fibers in the brush-tailed possum is presented in detail and discussed in comparison to placental forms already examINTRODUCTION ined. This represents the first such study of this system The principal neural inputs to the mammalian dorsal in a species of the order Marsupialia. column nuclei (DCN) are the ascending afferent nerve fibers which enter the central nervous system (CNS)via segmental dorsal roots. These fibers form part of the spinal dorsal columns (fasciculusgracilis [FG]and fasciculus cuneatus [FC]) which comprise the beginning of a major somatic afferent pathway to the brain in all orders of mammals. As such they subserve complex aspects of mechanoreceptive sensation, which depends on 'A dermatotopic (or segmentotopic) arrangement of nerve fibers (or subsequent transmission to brainstem and cerebral cor- cells) preserves and displays the topographic spinal relations that tex (Mountcastle, 1984), and they also carry ascending exist between fibers from different spinal nerves. A somatotopic patimplies a continuous three-dimensional map of the body surface proprioceptive information crucial to motor control tern which is organized via inputs from multiple spinal levels. (Hummelsheim et al., 1985; Rosen, 1969). These firstorder afferent projections traverse the dorsal columns in Received July 29, 1986.Accepted October 29, 1986. ABSTRACT This study describes the projection of cervical spinal afferent nerve fibers to the medulla in the brush-tailed possum, a marsupial mammal. After single dorsal roots (between C, and TI) were cut in a series of animals, the Fink-Heimer method was used to demonstrate the projection fields of fibers entering the CNS via specific dorsal roots. In the high cervical spinal cord, afferent fibers from each dorsal root form a discrete layer in the dorsal funiculus. The flattened laminae from upper cervical levels are lateral and those from lower cervical levels are medial within the dorsal columns. All afferent fibers at this level are separated from gray matter by the corticospinal fibers in the dorsal funiculus. All cervical roots project throughout most of the length of the well-developed main cuneate nucleus in a loosely segmentotopic fashion. Fibers from rostral roots enter more lateral parts of the nucleus, and fibers from lower levels pass to more medial areas; but terminal projection fields are typically large and overlap extensively. At more rostral medullary levels, fibers from all cervical dorsal roots also reach the external cuneate nucleus. The spatial arrangement here is more complex and more extensively overlapped than in the cuneate nucleus. Rostra1 cervical root fibers reach ventral and ventrolateral areas of the external cuneate nucleus and continue to its rostral pole; more caudal root fibers project to more dorsal and medial regions within the nucleus. These results demonstrate that projection patterns of spinal afferents in this marsupial are similar to those seen in the few placental species for which detailed data concerning this system are available. (91987 ALAN R. LISS, INC CERVICAL SPINAL AFFERENTS TO POSSUM DCN MATERIALS AND METHODS Experiments were done on a series of 15 adult brushtailed possums (Trichosurus vulpecula). Feral animals were collected by hand capture from the immediate environs of Dunedin, New Zealand. They were held approximately 3-5 days before use in experiments. Animals of both sexes (eight females, seven males) weighing from 2.7 to 3.9 kg were individually housed under outdoor ambient lighting conditions and fed ad libitum (dog food) before and after surgery. Animals were anesthetized by intraperitoneal injection with sodium pentobarbital (50-60 mgkg, supplemented as needed to maintain deep surgical anesthesia). Through a dorsal midline incision, the cervical spine and/or external surface of the occipital bone was exposed, and in each case, a different cervical spinal nerve was identified and isolated. Spinal levels sampled were C2-T1, with the exception of Cg. TI is included here because it is a large, brachial plexus root which, due to its peripheral distribution, has more in common with cervical roots than with other thoracic levels. After the spinal ganglion was exposed by enlarging the intervertebral foramen, the dura was opened and all dorsal rootlets of a single nerve were sectioned just central to the ganglion. Sterile Gelfoam was placed over the bony defect, and the wound was closed in two stages; muscle was closed with gut sutures, and the skin with silk. All demanding stages of surgery were performed under microscopic control. After 5 to 6 days postoperative survival (based on prior experience with this fiber system in several species; Culberson and Albright, 1984), animals were anesthetized as described above, injected (intracardiac) with 5,000 units of heparin, and killed by transcardiac perfusion with warm (28-30°C) 0.9% NaCl solution followed by a 10% formalin fixative solution. Brains and spinal cords were removed immediately and stored in fresh 10% formalin for 8 weeks to 6 months before further processing. Exact levels and completeness of dorsal root sections were verified at the time of cord removal. The medulla from each animal was blocked into one or two pieces, and each of these was frozen sectioned (40 pm thickness) serially in the transverse (11cases) or parasagittal (four cases) plane. Transverse sections at 0.24-mm intervals or alternate parasagittal sections were impregnated by using the Fink-Heimer (1967) procedure; an adjacent section in each case was stained with cresyl violet acetate. Drawings shown here were traced from projected images of actual sections;the exact location of degenerated fibers of passage (large dots in Figs. 1-5) and projection fields (small dots in Figs. 1-5) was filled in under microscopic control. principal target nuclei are relevant to the findings. The cuneate nucleus extends throughout the C1 spinal cord segment where it bulges into the base of the dorsal funiculus (Figs. 1-5, A and B). It increases in crosssectional area beginning about 1.5 mm below the obex; shifts laterally in position beginning at the obex; and at about 1.5 mm above this level, its cells display a more diffuse, reticular arrangement. The rostral end of the CN comes to lie adjacent to the EC rostral t o the obex. Cells of the CN are pale-staining, round and irregular multipolar neurons of medium size; some slightly larger, more intensely staining cells occur in the large part of the nucleus near the obex and scattered through its more caudal levels. The EC is easily recognized by its large, intensely stained, multipolar cells. It is first seen at obex levels as scattered neurons at the dorsolateral angle of the medulla. From there it expands in size and extends rostrally for about 4 mm (Figs. 1-5, D-F). Its medial border abuts on the rostral part of the CN. The Ascending Fibers Just above their spinal cord entry level, fibers from each dorsal root form a compact bundle of degenerated fibers in the lateral edge of FC. As they course rostrally, they spread into a larger area of FC and mix with adjacent normal fibers. Figure 6A shows an example of degenerated FC fibers. Fibers from most cervical dorsal roots tend to separate into two bundles, one medial and deep in the FC, the other more laterally and superficially placed (cf. Fig. 3A-C). There are differences in the distribution of fibers from these two bundles which may relate to different functions (see Discussion). Beginning at caudal medullary levels and continuing throughout the length of CN, terminals or collaterals of FC axons form small bundles which drop vertically through the FC and the pyramidal tract to reach their targets for distribution. Many axons from the lateral bundle continue rostrally, shift laterally, and finally extend directly into targets in the EC and the spinal trigeminal nucleus. Distribution of Upper Cervical Afferent Fibers (C2-C4} Degenerated fibers from these roots form adjacent, overlapping laminae in the lateral part of FC in the caudal medulla. Fibers from C2 are most lateral, with C3 (Fig. 1A) and then C4 (Fig. 2A) fibers medial to them. As fibers continue rostrally, separation into a deeper and a more superficial population is seen, most apparently in the C4 case Fig. 2B,C). Preterminal degeneration is seen to enter and distribute diffusely in the rostral RESULTS The principal results of this study are summarized by Figures 1-5, which illustrate the course and medullary distribution of the dorsal root fibers degenerated after rhizotomy in five representative experimental cases. The following text treats features common to projections from all spinal cord levels and points out differences among projections of different dorsal roots. Architecture of Medullary Target Nuclei 233 aP C cn ec fc fg g h i m P S Although we did not undertake cytoarchitectural t n analysis of the possum medulla, brief comments on the tt Abbreviations area postrema central cervical nucleus nucleus cuneatus external cuneate nucleus fasciculus cuneatus fasciculus gracilis nucleus gracilis hypoglossal nucleus nucleus intercalatus dorsal motor nucleus of vagus pyramidal tract fibers solitary complex (nucleus and tract) spinal trigeminal nucleus spinal trigeminal tract Fig. 1. Drawings of the dorsolateral quadrants of sections through the medulla of a possum with a C3 dorsal root lesion. Sections shown are spaced at approximate 1.25-mm intervals and are arranged from caudal (A) to rostra1 (F). In this and subsequent figures, large dots represent fibers of passage; small dots represent apparent projection fields or terminal fields of fibers. CERVICAL SPINAL AFFERENTS TO POSSUM DCN c4 Fig. 2. Drawings of the dorsolateral quadrants of sections through the medulla of a possum with a C4 dorsal root sesion. Sections shown are spaced at approximate 1.25-mm intervals and are arranged from caudal (A) to rostra1 (F). 235 236 J.L. CULBERSON Fig. 3. Drawings of the dorsolateral quadrants of sections through the medulla of a possum with a C, dorsal root lesion. Sections shown are spaced at approximate 1.25-mm intervals and are arranged from caudal (A) to rostra1 (F). CERVICAL SPINAL AFFERENTS TO POSSUM DCN Fig. 4. Drawings of the dorsolateral quadrants of sections through the medulla of a possum with a C7 dorsal root lesion. Sections shown are spaced at approximate 1.25-mmintervals and are arranged from caudal (A) to rostra1 (F). 237 238 J.L. CULBERSON Fig. 5. Drawings of the dorsolateral quadrants of sections through the medulla of a possum with a T, dorsal root lesion. Sections shown are spaced at approximate 1.25-mm intervals and are arranged from caudal (A) to rostra1 (F). CERVICAL SPINAL AFFERENTS TO POSSUM DCN 239 Fig. 6 . Photomicrographs showing characteristic appearance of de- caudal nucleus cuneatus, adjacent to cuneate fasciculus. This is on the generated axons and terminals in the medulla. A: Fibers in medial medial side of the nucleus after a C6 dorsal root section. D: Slightly fasciculus cuneatus following C8 dorsal rhizotomy. Nearly all fibers ex- coarser, less-dense debris in the ventrolateral part of the nucleus cuneahibit a coarse, beaded appearance. 8: Dense, coarse preterminal debris tus from the same section as C. Fink-Heimer stain; bar in C = 50 pm for surrounding large neurons in the medial part of the external cuneate all figures. nucleus after C7 lesion. C: Fine, granular debris in the dorsal shell of the end of the central cervical nucleus (C), and in caudal sections through C1 there are extensive endings in the adjacent reticular formation. This is especially true for the C2 and C3 (Fig. 1A) cases, where this projection is an extension of the typically heavy afferent fiber distribution to spinal intermediate gray matter. Within the caudal CN, fibers from Cz project to the extreme lateral edge of the nucleus and generate a large preterminal field in the ventrolateral part of the CN; this projection resembles that shown in Figure 6D. Fibers from C3 and C4 have similar distribution; they are most expansive in the deeper ventrolateral area of CN (Figs. lA,C, 2A,C) and have a small projection t o the lateral, superficial zone. At obex levels, all three of these roots (Cz-C,) send a projection to the superficial dorsal portion of the spinal trigeminal nucleus (Figs. 1D,E; 2D). This extends far ventrally in the C3 case but in all cases has a very limited rostrocaudal extent. Fiber projections to the EC are extensive; rostrally coursing fibers from C2 and C3 lie just ventral t o the EC 240 J.L. CULBERSON mixed with fibers of the spinal trigeminal tract. Their endings are in the extreme ventral and ventrolateral areas of the EC throughout its length, although with a heavier projection to its rostral end than more caudally (Fig. 1D-F). The C4 distribution to the EC arises from fibers passing forward in this same location and from fibers of the superficial bundle, which lies at the dorsomedial edge of the nucleus (Fig. 2D-F). The target for C4 fibers is more caudally placed than that for Cz and C3, in the central and medial areas of the ventral onethird of the EC. Distribution of midcervical afferent fibers (C5, C6) Since a C5 case is lacking in this study, these midcervical levels are represented by Figure 3, which was drawn from a representative C6 case. There continues to be a diffuse projection to the central cervical nucleus (Fig. 3A) from Cg. The CN in this case receives a dense projection to well-defined areas of its superficial shell (Fig. 6C); these fibers arise mainly from the more medial of the two recognizable bundles in the FC. This input to the CN is medial to the high cervical input to the CN and is concentrated in the dorsal superficial part of the nucleus (Fig. 3A,C,D), although there is some shifting in location (Fig. 3B). There is a second projection field in the deeper, ventrolateral CN which is well developed throughout all but the rostral end of the nucleus. These fibers enter from the larger, lateral bundle in the FC and end by overlapping the same area as in C 4 4 cases. The EC receives input mainly from the lateral FC bundle which lies at the EC-CN interface (Fig. 3D) and just dorsal to the EC. Fibers in the ventral EC end in the center of the nucleus at caudal levels; more rostrally their large terminal field shifts dorsally into the center of the nucleus. A few fibers extend to the rostral end of the EC to central and lateral areas. Distribution of more caudal cervical afferent fibers (C7-T,) Fibers from these dorsal roots form flattened to crescentic laminae in the extreme medial FC when viewed in cross section in the caudal medulla (Figs. 4A,B; 5A,B). As they continue rostrally some fibers retain this relative position while many shift laterally in a superficial location in FC. The central cervical nucleus receives a minimal input in the C7 case but contains no degenerated fibers following Cs or T1 lesions. Fiber projections to the caudal CN arise as collaterals or terminals of the more medial FC fibers; these radiate toward the nucleus from several directions (Figs. 4A; 5B,C) to reach and ramify among the superficial cells of the CN. This projection to dorsal CN is extensive from C7 and Cs and extends to multiple targets, especially along the medial edge of the CN (Fig. 4B,C). T1 also projects to multiple sites in the shell of CN. These three roots also send many fibers into the deep ventrolateral area of NC where other cervical roots project. This latter system arises from the large, laterally situated FC bundle, which also projects more rostrally into the EC. Within the EC, C7 fibers reach large target areas; a small projection goes caudal and ventral, more fibers spread out through the dorsal one-half of EC at its largest extent, and the heaviest projection is to its medial midregion (Figs. 6B, 4D). Few fibers extend into the rostral quarter of EC. The Ti root sends fewer fibers into the EC, where they end in its dorsal one-half (Fig. 5E,F). DISCUSSION The brush-tailed possum is a cat-sized, diprotodont marsupial with a strong, thick neck; large, mobile ears; and a large, furry tail. The animal is largely arboreal and moves quickly and with great agility through the trees. It possesses very strong limb (especially forelimb) musculature and displays reasonable but not facile dexterity in manipulation of objects with the forepaws (see Ride, 1970, for more details). Although few studies of somatosensory pathways in this or other Australasian marsupials have been published, Clezy et al. (1961) and Dennis and Kerr (1961)have demonstrated the presence of major classical pathways (dorsal column-medial lemniscus and anterolateral systems) in the brainstem in Trichosurus. The forebrain components of these pathways that relate thalamus and cortex in this species have also been studied by Rockel et al. (1972)and Haight and Neylon (1978); and, a t least in general outline, they resemble the placental arrangement. Since neither the primary afferent nor the spinomedullary tracts have been examined, the present data are considered in relation to the few studies on American marsupials @idelphis sp.) and the more extensive work on several placental forms. The qualitative observations included here concerning cytoarchitecture and nuclear subdivisions of DCN are necessarily preliminary in nature as they rely only on Nissl material and some data concerning afferent fiber projections. Two longitudinal zones are differentiateda rostral reticular area, beginning 1-5 mm rostral to the obex, and the remaining caudal zone which extends down through the medulla and the C1 spinal segment. This breakdown coincides with the developmental description of the CN provided by Ulinski (1969) for the opossum and with other authors’ description of the CN in the rat (Basbaum and Hand, 1973) and cat (Kuypers and Tuerk, 1964; Keller and Hand, 1970). The caudal region in Trichosurus is enlarged in size for about 1.5 mm above and below the obex, and although there is little obvious change in cytology and cell density (in our Nissl-stained sections), this is the area which corresponds to the third subdivision of the CN described in most detailed cytoarchitectural studies (Albright and Haines, 1978, bushbaby; Albright et al., 1983, squirrel; Biedenback, 1972, rhesus monkey; Cheema et al., 1983, cat; Penny, 1982, opossum). This obex region is likely to be the major target for low-threshold cutaneous afferents from the forepaw (see below);but in the brush-tailed possum, it is not obviously distinguished by presence of cell “clusters” (Keller and Hand, 1970; Kuypers and Tuerk, 19641, “bricks” (Basbaum and Hand, 19731, or cell “columns” (Albright and Haines, 1978). There also is no separation into obvious subnuclei as in the monkey (Cheema et al., 1983; Ferraro and Barrera, 1935; Rustioni et al., 1979). Dorsal root fibers generate a dual projection to the CN up to the rostral zone, where projections are most diffuse. Fibers reaching the dorsal “shell” of the nucleus, which produce fine, dense debris (Fig. 6C), comprise the topographically precise projection. Their arrangement is in accordance with classic descriptions in rat (Basbaum and Hand, 19731, cat (Kodama, 1942; Rustioni and Macchi, 1968), squirrel (Albright et al., 1983), and primates (Albright and Haines, 1978; Ferraro and Barrera, 1935; Rustioni et al., 1979; Shriver et al., 1968; Walker and CERVICAL SPINAL AFFERENTS TO POSSUM DCN Weaver, 1942). Mapping studies of DCN cell responses to peripheral stimulation in several species confirm this general arrangement and show that input to this dorsal part of the nucleus is derived from cutaneous mechanoreceptors which are most numerous in those roots which innervate the distal extremity or forepaw (Dykes et al., 1982;Hamilton and Johnson, 1973; Johnson et al., 1968; Kruger et al., 1961; Millar and Basbaum, 1975). This observation also has been supported recently by anatomical studies showing cutaneous nerve distribution to the dorsal (and central) part of the CN in cat (Nyberg and Blomqvist, 1972). In the present material, there was a more extensive projection to the dorsal CN from presumed distal (paw)dermatomes (C7-Tl)2 than from proximal ones, and a minimal projection from dermatomes presumed to supply the neck and shoulder (CZ-C~). There is also more mediolateral overlap of the projections of adjacent root fibers in Trichosurus than some authors have reported in other mammals. The second NC target for spinal afferent fibers is the ventrolateral/ventrocentral region to which all cervical roots send an overlapping projection of coarse, degenerated fibers (Fig. 6D). These fibers arise from the large lateral bundle of FC and are abundant throughout all but the most rostral part of the CN. They are likely to be low-threshold muscle afferents, according t o mapping studies (Rosen, 1969); and appropriately, they are relatively more expansive in CZ-C~cases than from C7 and Cs. Support for this spatial modality segregation (and localization) of muscle afferents comes from the recent studies by Nyberg and Blomqvist (1983) in the cat and by Hummelsheim et al. (1985) for projections to the homologous region (pars triangularis) in the monkey CN. The final major medullary target for primary afferents is the EC, which is well known to receive muscle afferents (Kruger and Norton, 1973). In the brush-tailed possum, this projection is a large one from all cervical roots; and, although adjacent root projection fields overlap extensively, a clear segmentotopic pattern is seen. It concurs in general with that shown by Liu (1956) in his excellent early study of this nucleus in cat. The elegant muscle-to-EC mapping study by Campbell et al. (1974) in rat indicates a rostral EC target for neck musculature (our C2-C4 roots had heaviest rostral projection) and spatially well-defined areas for fibers from arm, hand, forearm, and shoulder. Our results, assuming typical dermatomal representation (see footnote 21, fit reasonably well with their schema of forelimb representation in the EC. We expect some variation based on the differences in dermatomes and limb usage; and, in addition, dorsal root projections to the EC also convey some cutaneous aflerents intentionally excluded from consideration by Campbell et al. (1974). Given the behavioral repertoire of the brush-tailed possum (see above), it is not surprising to find in an anatomical study of the dorsal column system a very extensive, well-developed cuneate system. The FC is in 241 fact very large compared to the gracile component of the dorsal column system in this species. Within the cuneate projections are many fibers which distribute to portions of the CN and EC known to receive proprioceptive inputs. Projections to the dorsal CN, especially in the region near the obex, are abundant; but neither the cells in CN nor the fiber projection seem to be arranged so precisely as those in placental mammals (primates) with well-developed digital dexterity (Albright and Haines, 1978; Culberson and Albright, 1984;Rustioni et al., 1979). ACKNOWLEDGMENTS Experimental material upon which this report is based was colIected while the author was Visiting Senior Lecturer in the Department of Anatomy at University of Otago, Dunedin, New Zealand. I am very grateful for facilities, friendship, and assistance graciously provided by many members of that department, especially Len Robinson, then Acting Chairman, and C.J. Heath. Excellent technical assistance in Dunedin was provided by Mr. Ken Turner; and histologic processing (at WVU) was by Sue Horvat, Dorothy Heritage, and Debbie McIntosh. Donna Borland typed the manuscript. Some of these data have been reported in abstract form (Culberson, 1979; Culberson et al., 1983). The work was supported in part by grants from the West Virginia Medical Corporation-USPHS (5-Sol-RRO5433) and NSF (BNS 5792472). LITERATURE CITED Albright, B.C., and D.E. Haines 1978Dorsal column nuclei in a prosimian primate (Galago senegalensis). 11. Cuneate and lateral cuneate nuclei: Morphology and primary afferent fibers from cervical and upper thoracic spinal segments. Brain Behav. Evol., 15:165-184. Albright, B.C., J.I. Johnson, and E.M. 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