Cytoplasmic laminated bodies in the visual cortex of the cat

Cytoplasmic laminated bodies in the visual cortex of the cat

544 Brain Research, 161 (1979)544 548 ~i) Elsevier/North-Holland Biomedical Press Cytoplasmic laminated bodies in the visual cortex of the cat D. A...

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544

Brain Research, 161 (1979)544 548 ~i) Elsevier/North-Holland Biomedical Press

Cytoplasmic laminated bodies in the visual cortex of the cat

D. A. WINFIELD

Department of Human Anatomy, Oxford, OX1 3QX (U.K.) (Accepted October 19th, 1978)

Complex cytoplasmic laminated bodies (CLBs) as inclusions in neuronal somata have been described in a number of systems and species. Most commonly, they have been reported in neurones of the visual system: in horizontal cells in the human retinal4; in the lateral geniculate nucleus of the cat~,s,l°-12; and in the striate cortex of the monkey 6. They are not, however, specific to the visual system because they have been found in other sites such as the cortex 9 and deep nucleP 3 of the cerebellum, and in the ventrobasal and posterior nuclei of the thalamus 3. N o r are CLBs to be seen in every nucleus of the visual pathway: they are apparently absent from the superior colliculus and the ventral geniculate nucleus in the cat 5. As it has been suggested ~,6 that CLBs are not present in the visual cortex of the cat and because it is possible that they are found only in certain types of cells in the lateral geniculate nucleus 8, evidence is presented about a small number of neurones with CLBs in area 17 of the cat. The cortex of area 17 of 13 cats has been examined with the electron microscope in a study of the postnatal development of the cortex in normal kittens and kittens with unilateral or bilateral eyelid closure. The animals had been perfused at 24 °C with a mixture of 4 ~ paraformaldehyde and 1 ~ glutaraldehyde after a brief wash out with a balanced salt solution. Blocks cut coronally from the visual cortex in the medial wall of the lateral gyrus were processed for electron microscopy and after examination of 1 # m thick sections stained with toluidine blue, ultra-thin sections were obtained through the depth of the cortex. In addition, similar material from the cortex of area 17 of 3 monkeys has been studied; the brains had been fixed and processed as for the cat. CLBs have been found in 17 neurones in area 17 of the cat and in 7 of the monkey. They consist of curved parallel arrays (Figs. 1-5) of thick-walled tubules of 25 nm diameter separated by granular dense material approximately 75 nm wide1,1°. They are of the same order of size as nucleoli and the tubules swirl to form a structure °resembling a fingerprint '12. CLBs may be related to or apparently contiguous with cisternae of endoplasmic reticulum or mitochondria (Fig. 5) and there may be one or two islands of cytoplasm in them. They are very similar to those observed in the feline lateral geniculate nucleus. All the neurones with CLBs had essentially the same electron microscopic features. They were small and round or oval with few synapses

Fig. 1. A neurone with a complex laminated body (arrow) from lamina IV of the visual cortex in a kitten 70 days of age. The neurone is oval with a round indented nucleus and a moderate amount of cytoplasmic organelles; it lacks an apical dendrite and an asymmetric synapse in this section, x 6750. Fig. 2. The complex laminated body from the neurone in Fig. 1 at a higher magnification. The dark lines are sheets of tubules, sectioned transversely on the left and longitudinally on the right. Electrondense material forms the intervening dark layers which together with the tubules whorl to give a structure resembling a fingerprint in cross-section. × 14,300. Fig. 3. A complex laminated body from the cytoplasm of a neurone in lamina IV of the visual cortex of an adult cat (415 days). Mitochondria (m) are closely associated with the body which contains an island of cytoplasm, x 25,000.

Fig. 4. A n e u r o n e with a c o m p l e x laminated body (arrow) in l a m i n a IV o f the visual cortex o f a cat aged 110 days. T h e n e u r o n e is virtually r o u n d with an indented nucleus. Its nucleolus is present a n d a l t h o u g h it is sectioned centrally it lacks an apical dendrite in this plane. ,, 7750. Fig. 5. T h e c o m p l e x laminated body f r o m the n e u r o n e in Fig. 4 seen at higher magnification. G r a n u l a r e n d o p l a s m i c reticulum (e.r.) is associated with the body a n d there are several islands of c y t o p l a s m within it. m ~: m i t o c h o n d r i o n , x 24,500.

547 TABLE I The number o f cells with CLBs observed at different ages in the cat

The number of cells with CLBs and the laminae (in parentheses) in which they occurred for normal cats of different ages and cats with varying periods of monocular or binocular eyelid suture, n.a. = not available. Age (days)

40 70 110 200 Adult

Normal

Eyelid suture Monocular

Binocular

1 (II) 0

0 0

1 (IV)

4 (IV)

0

n.a. 3 (IV)

n.a. 4 (IV) 2 (IV)

1 (IV) n.a.

0 1 (IV)

upon their surfaces, all of which were symmetric. Cells with CLBs in the cat had a mean diameter of 14.8 4- 0.5 # m and were significantly larger than those in the monkey which had a mean diameter of 9.8 4- 0.5/zm. In several cells the nucleus had an irregular outline with a number of indentations. The cells lacked an apical dendrite, characteristic of pyramidal neurones, even when cut centrally as judged by the presence of a nucleolus and with the sections aligned perpendicular to the surface; there were many other neurones in the supra- and infragranular layers that had apical dendrites and were clearly pyramidal. All but one of the neurones in the cat and all those of the monkey were in lamina IV, which is similar to the findings of Kruger and Maxwell 6 who stated that they were in or near the granular layer. The one cell with a CLB that was not within layer IV in the cat was in layer II in a 40-day-old kitten with unilateral eyelid closure; the neurone had features very similar to those cells with CLBs seen in layer IV. The absence of an apical dendrite from the neurones with CLBs suggests that they are not pyramidal cells, and the relatively small amount of cytoplasm and the small number of synapses distinguish them from the non-pyramidal or stellate cells described by Colonnier 2 and Jones and Powell 4. It is possible that they form a distinct class of non-pyramidal neurone with only symmetrical synapses upon their somata as has been described in the visual cortex of the cat and monkey 7. However, until a larger number of cells with CLBs has been studied, particularly in serial sections to determine whether asymmetric synapses or an apical dendrite are present, it would be premature to conclude that they occur in a single cell-type in the visual cortex. Rearing kittens in the dark causes more neurones to form CLBs in the lateral geniculate nucleusZ. In the present study, CLBs have been seen in the visual cortex of normal cats and kittens with unilateral or bilateral eyelid suture, but the small size of the sample does not permit reliable estimates of any differences between the normal and experimental animals. CLBs have not been encountered in kittens with bilateral eyelid suture before the age of 200 days (see Table I), but this apparent delay in the development of CLBs after bilateral lid suture would not necessarily be significant - -

548 as H e r m a n and R a l s t o n a have p o i n t e d out that while they had observed 46 cells with CLBs in the t h a l a m u s of the cat, two-thirds of them were in one animal a n d 6 animals had none. N e u r o n e s with CLBs in the p r i m a r y visual cortex of the cat are rare a n d p r o b a b l y form less t h a n l ~ of the cells - - thus m a k i n g it difficult to d e m o n s t r a t e them especially at the electron microscopic level. If they are present with the same frequency in cells in other systems a n d species, it is n o t surprising that they have been described so infrequently. This work was supported by grants from the Medical a n d Science Research Councils.

1 Barron, K. D., Doolin, P. F. and Oldershaw, J. B., Ultrastructural observations on retrograde atrophy of lateral geniculate nucleus. I. Neuronal alterations, J. Neuropath exp. Neurol., 26 (1967) 300-326. 2 Colonnier, M., Synaptic patterns on different cell types in the different laminae of the cat visual cortex, Brain Research, 9 (1968) 268-287. 3 Herman, M. M. and Ralston, H. J., Laminated cytoplasmic bodies and annulate lamellae in the cat ventrobasal and posterior thalamus, Anat. Rec., 167 (1970) 183-196. 4 Jones, E. G. and Powell, T. P. S., Electron microscopy of the somatic sensory cortex of the cat. I. Cell types and synaptic organization, Phil. Trans. B., 257 (1970) 1-41. 5 Kalil, R. and Worden, I., Cytoplasmic laminated bodies in the lateral geniculate nucleus of normal and dark reared cats, J. comp. Neurol., 178 (1978) 469-486. 6 Kruger, L. and Maxwell, D. S., Cytoplasmic laminar bodies in the striate cortex, J. Ultrastruct. Res., 26 (1969) 387-390. 7 Le Vay, S., Synaptic patterns in the visual cortex of the cat and monkey. Electron-microscopy of Golgi preparations, J. comp. NeuroL, 150 (1973) 53-86. 8 Le Vay, S. and Ferster, D., Relay cell classes in the lateral geniculate nucleus of the cat and the effects of visual deprivation, J. comp. Neurol., 172 (1977) 563-584. 9 Morales, R. and Duncan, D., Multilaminated bodies and other unusual configurations of endoplasmic reticulum in the cerebellum of the cat. An electron microscopic study, J. Ultrastruct. Res., 15 (1966) 480-489. l0 Morales, R., Duncan, D. and Rehmet, R., A distinctive laminated cytoplasmic body in the lateral geniculate body neurons of the cat, J. Ultrastruct. Res., 10 (1964) 116-123. 11 Peters, A. and Palay, S. L., The morphology of laminae A and A1 of the dorsal nucleus of the lateral geniculate body of the cat, J. Anat. (Lond.), 100 (1966) 451-486. 12 Smith, J. M., O'Leary, J. L., Harris, A. B. and Gay, A. J., Ultrastructural features of the lateral geniculate nucleus of the cat, J. comp. Neurol., 123 (1964) 357-378. 13 Sotelo, C. and Angaut, P., The fine structure of the cerebellar central nuclei in the cat. I. Neurons and neuroglial cells, Exp. Brain Res., 16 (1973) 410-430. 14 Villegas, G. M. and Yoshida, M., Referred to as unpublished work by Morales et al. (1964).