Complex convolutions in neurons of the dorsal lateral geniculate nucleus of the normal albino rat

Brain Research, 4114(1987) 231-238

231

Elsevier BRE 12373

Complex convolutions in neurons of the dorsal lateral geniculate nucleus of the normal albino rat Jorge Satorre*, Carmen de |a Roza, Josefina Cano and Fernando Reinoso-Sufirez Departamento de Morfologia, Facultad de Medicina, Univ °~;,4.,,4 a ,-,~oma de Madrid, Madrid (Spain)

(Accepted 8 July 1986) Key words: Complex convolution; Dorsal lateral geniculate nucleus; Rat

The postnatal development of complex convolutions (CCs) of the dorsal lateral geniculate nucleus (LGNd) in normal rats has been studied quantitatively with light microscopy. We report that immature neurons do not contain these scarcely understood organelles, since they can be seen for the first time in very few, mature neurons of the 30 day rat; their number constantly increases during the following 4 months. These cytoplasmic inclusions can be equally seen in the aged rat. CCs are present in neurons of all sizes, except the smallest, which correspond to the interneuron population. Although, morphologically, CCs of the LGNd of the rat are similar, but not identical, to the cytoplasmic multilaminated bodies of the cat, intermediate forms are described.

INTRODUCTION A p r o m i n e n t characteristic of a great part of the neurons of the dorsal lateral geniculate nucleus ( L G N d ) , when they are seen in semithin sections, is the presence of basophillic cytoplasmic inclusions, of an ovoid morphology, similar in size to the nucleolus. These bodies, which were ultrastructurally described for the first time in the L G N d of the cat by Morales et al. 33 and later confirmed by Smith et al. 47, Peters and Palay 38, and B a r r o n et al. 2, were called 'cytoplasmatic laminar bodies' (CLBs), because they were c o m p o s e d of regularly repeating dark and lighter lines, often arranged in whorls, resembling fingerprints. The CLBs are structures of a complex chemical composition, f o r m e d mainly by proteins and, to a lesser degree, by lipids and polysaccharides, but with no nucleic acids 6. The function and origin of these complex organelles is unknown, although they have been related

to the endoplasmic reticulum 2'6'33"47'48. However, these p r o b a b l e specializations of the endoplasmic reticulum are resistant to transneuronal cell change associated with denervation 2'47. The presence and distribution of the CLBs in the diverse subcortical nuclei and cortical areas of the central nervous system of the various species studied are very variable; most c o m m o n l y they have been rep o r t e d in the cat and in neurons of the visual system. They have been m o r e frequently described and studied with greater detail in the L G N d of the cat 2'6'10'19'20'25'33'38'45'47. H o w e v e r , no laminated inclusion b o d y has been found in the neurons of the L G N d of the m o n k e y 16'55, of the night-active primates t4, of the s u b p r i m a t e Tupaia glis J3 or of the rabbit 11. Similarly, Kalil and W o r d e n 2° have never seen a CLB in the ventral lateral geniculate nucleus or in the superior colliculus of the cat. CLBs have been seen in a small percentage of neurons of the striate cortex of the m o n k e y 23'54 and of the cat 54, but none have been found in other cortical

* Present address: Servicio de Oftalmologfa, Hospital del INSALUD, Yecla (Murcia), Spain. Correspondence: F. Reinoso-Sufirez, Departamento de Morfologfa, Facultad de Medicina, Universidad Aut6noma de Madrid, Ar-

zobispo Morcillo 2, 28029 Madrid, Spain. 0006-8993/87/$03.50 © 1987 Elsevier Science Publishers B.V. (Biomedical Division)

232 fields of the m o n k e y 23. O t h e r than in the visual system, CLBs have been identified, in the cat, in other sites such as the cerebellar cortex 32, in the ventrobasal and posterior thalamus Is and in the d e e p nuclei of the cerebellum 48. Similar bodies, but not morphologically identical, were described in the neurons of the L G N d of the rat by Karlsson 21, who called such cytoplasmic inclusions 'complex convolutions' (CCs) and described them as a complex of m e m b r a n e b o u n d tubules. Later, Lieb e r m a n et al. 2s confirmed the presence and structure of these bizarre m e m b r a n o u s specializations in the rat L G N d , besides finding them as well in the ventrobasal nuclear complex and pars lateralis of the posterolateral nuclear complex. On the other hand, Kruger and Maxwell 23 did not find a single CC in the visual cortex of the rat and Rafols and Valverde < did not describe any in the L G N d of the mouse. Descriptions of CCs have always been m a d e in adult rats. While studying the d e v e l o p m e n t of geniculate cells in the rat, we noted that i m m a t u r e neurons did not contain these cytoplasmic inclusions, as did mature ones. To investigate this p r o b l e m in detail, we have u n d e r t a k e n a quantitative analysis of CCs in the normal rat L G N d during postnatal d e v e l o p m e n t and aging. A t t e n t i o n has been paid to measuring the diameter of neurons containing CCs in relation to the neuronal population. MATERIALS AND METHODS A total of 14 healthy S p r a g u e - D a w l e y albino rats were studied: two each of ages 0, 10, 20, 30, 90 and 165 days, and one each of ages 29 and 31 months. U n d e r ether anesthesia the rats were perfused intracardially for 5 min with 0.9% saline (4 °C) followed immediately by 30 min perfusion with 50-15(1 ml (depending on the age of the rat) of fixative containing 1% p a r a f o r m a l d e h y d e , 1.5% glutaraldehyde and 0.1% CaC12 in 0.1 M sodium cacodylate buffer (pH 7.2), followed by 50-150 ml of a second fixative containing 2% p a r a f o r m a l d e h y d e , 3% glutaraldehyde and 0.1% CaC12 in the same buffer. The brains were r e m o v e d from the skulls and i m m e r s e d in the second fixative. The duration of the immersion fixation d e p e n d e d on the age of the animal: from newborn to 30-day-old, immersion continued for 8 days; at 3, 5.5, 29 and 31 months old, 18 h was suffi-

cient. Thereafter, all tissue was rinsed in 0.1 M sodium cacodylate buffer. Tissue pieces, from the optic chiasm to the superior colliculus, were m o u n t e d on Lancer 1000 v i b r o t o m e stages, and 100/,m thick coronal sections were cut into the sodium cacodylate buffer to aid localization, orientation and fixation of the L G N d . Subsequently, the L G N d and adjacent areas were dissected from each section using a stereomicroscope and the aid of a fine brush and microsharp blade. To complete the processing for miscroscopy, the tissue was postfixed for 1 h with 2% osmium tetraoxide in 0.1 M sodium cacodylate buffer, d e h y d r a t e d in a graded series of alcohols and emb e d d e d in E p o n 812. Serial sections of 0.9/~m thickness were cut with glass knives from the 100 Bm sections using a Sorvall MT-5000 u l t r a m i c r o t o m e , and stained with toluidine blue. Ultrathin sections of 600-800 ,~. were stained with uranyl acetate in methanol and lead citrate before they were observed in a Philips 301 electron microscope. One out of every 30 semithin sections (0.9 Bm) of the L G N d at different ages was p r o j e c t e d with a camera lucida at 40 x magnification, drawn, and each area measured by an HP 9815 A/S Calculator-9874 A Digitizer; thereafter, the m e a s u r e d areas were reduced to their real value. Afterwards, we counted the nucleoli and the CCs of the whole area of these sections with a 100 x oil immersion objective. W e have tried to provide an accurate estimate of the true n u m b e r of CCs in the rat L G N d by counting each one regardless of w h e t h e r it was located in a dendrite or a cell body, since many CCs are located eccentrically. A l t h o u g h multiple nucleoli are a characteristic feature of neuronal d e v e l o p m e n t , when more than one nucleolus was a p p a r e n t in a single cell, only one was counted. The total number of CCs and nucleoli was then divided by the area of the L G N d to obtain a measure of CC and nucleolus density. Table | lists the correction factors calculated with A b e r c r o m b i e ' s formula 1, considering our units of counting as spheres. The data in Table II are derived from the uncorrected counts of nucleoli and CCs; corrected values may be obtained by applying the correction factors given in Table I. Cell d i a m e t e r histograms were p r e p a r e d to show the size distribution of cell; to find the mean value for the diameter of neuronal bodies we p r o c e e d e d in the

233 following way: only neurons with visible nucleolus were sampled and it was assumed that the nucleolus was centrally placed within its nucleus, and any profile which contained an evident nucleolus could therefore be r e g a r d e d as passing through the center of the nucleus. H e n c e the d i a m e t e r of any such profile represented the diameter of the neuronal body. It was estimated by measuring the p e r i m e t e r by an H P 9815 A/S Calculator-9874 A Digitizer, and dividing it by 3.1416. W e sampled at r a n d o m , at each age, 75 neuronal bodies containing a CC and 225 neuronal bodies without CC. We have quantified, as well, the percentage of neurons containing two CCs. RESULTS CCs, which m a y be several microns in diameter, a p p e a r as dark bodies in the cytoplasm of a great part of the neurons in the rat L G N d (Figs. 1 and 2); their most usual morphology, using the staining p r o c e d u r e described for light microscopy, appears to be elliptical, although differently shaped CCs as cigar-shaped, spherical or irregularly shaped, were also o b s e r v e d

Fig. 2. A: neuron with two CCs. B: irregular CC with a cytoplasmic invagination. C: spheroidal CC eccentrically located. D: very large oval CC. All pictures × 1330. (Figs. 1 and 2). The location of these complex inclusions in the neuronal cytoplasm is very liable to vary;

Fig. 1. Partial view of the LGNd of a 5.5-month-old rat. CCs (arrows) can be seen placed, either in the plane of the nucleus (with or without a nucleolus), or eccentrically. (x 590).

234

Fig. 3. A: CC showing, besides the typical structure of membrane bound tubules associated with balls of electron dense material, areas of curved parallel arrays of dark and gray rows (curved arrow). I~,, endoplasmic reticulum. 5.5-month-old rat; x 29,000. B: typical CC. I~, endoplasmic reticulum. 29-month-old rat; × 26,000.

we find them, now in the perikaryon, now in the main dendrites (Figs. 1 and 2). A small percentage of neu-

bodies (Fig. 3B). These types of m e m b r a n o u s specializations are occasionally found to be in continuity

rons, 1.82%, shows two CCs (Fig. 2A). Using electron microscopy, the type of CC most frequently found is made up of an ensemble of small subunits of coiled m e m b r a n e s associated with dense

with endoplasmic reticulum (Fig. 3A, B). In a smaller a m o u n t of cases, we can see CCs in which, besides the above m e n t i o n e d structure, one can see areas composed of parallel layers or m e m b r a n e giving the appearance of alternate dense and less dense bands, resembling the structure of the CLBs of the cat 33 (Fig. 3A).

TABLE I Correction factors for nucleoli and for CCs calculated by means of Abercrombie's formula Age 0 days 10 days 20 days 30 days 3 months 5.5 months 29 months 31 months

Rat

Correctionfactor for nucleoli

Correctionfactor ~br CCs

1 2 1 2 1 2 1 2 1 2 1 2 1 1

0.290 0.287 0.244 0.251 0.240 0.238 0.238 0.239 0.226 0.230 0.227 0.231 0.249 0.261

0.249 0.253 0.218 0.222 0.253 0.265

The immature neurons do not have CCs in their cytoplasm; these can be first seen in very few neurons of the 30-day-old rat. From this age onwards, these cytoplasmic inclusions are always present, their density being variable in all the rats studied. Nucleoli density decreases exponentially throughout the postnatal life of the rat (Table II). The n e u r o n population is quite homogeneous as to soma characteristics visible in semithin section preparation in the rat, with the exception of soma size (Fig. 1). Cell diameter histograms show that the only neurons which do not have CCs are the smallest sized neurons (Fig. 4). We d o n ' t think that these data are influenced by the error due to carrying out cell size measurements in the plane of the nucleolus, systematically excluding the neurons with their CCs out of the

235 DISCUSSION

TABLE II Nucleolar and complex convolution (CC) density in the dorsal lateral geniculate nucleus of the rat Rat

Age

0 days

1 2 1 2 1 2 1 2 1 2 1 2 1 1

10 days 20 days 30 days 3months 5.5months 29months 31months

CCs of the rat, s e e n t h r o u g h light m i c r o s c o p y are

Nucleoli per mm 2

CCs per mm 2

cytoplasmic inclusions similar to the m u l t i l a m i n a t e d bodies d e s c r i b e d in the cat 33. H o w e v e r , as K a r l s s o n 21

X

X

Range

already p o i n t e d o u t , the d i f f e r e n c e s that are ob-

0 0 0 0 0 0 * * 19 30 69 55 7 40

(12-43) (13-48) (43-103) (38-89) (0-11) (26-52)

Range

668 590 226 252 165 153 105 101 78 84 86 82 70 83

(419-921) (390-811) (170-280) (165-310) (129-190) (118-179) (84-136) (75-125) (59-99) (35-108) (55-105) (35-92) (42-120) (53-118)

s e r v e d ultrastructurally with respect to p a c k i n g of the t u b u l a r structures w a r r a n t the conclusion that the two organelles are similar but n o t identical. C C ultrastructure m o s t f r e q u e n t l y f o u n d by us coincides with the o n e d e s c r i b e d by K a r l s s o n 21 and L i e b e r m a n et a1.28: c o m p l e x of m e m b r a n e

b o u n d tubules asso-

ciated with balls of e l e c t r o n d e n s e m a t e r i a l , occasionally f o u n d to be in c o n t i n u i t y with c o n v e n t i o n a l end o p l a s m i c r e t i c u l u m (Fig. 3 B ) ; but we s o m e t i m e s find CCs such as t h o s e in Fig. 3 A , in which, besides the typical structure

* In 30-day rat number 1, 7 neurons were found with complex convolutions, whereas in rat number 2 only 5 were found.

of C C of t h e rat d e s c r i b e d

a b o v e , we see areas of layers of m e m b r a n e giving the a p p e a r a n c e of a l t e r n a t e d a r k and gray bands, similar to m u l t i l a m i n a t e d b o d i e s of t h e cat 33 and m o n k e y 23. T h e s e C C i n t e r m e d i a t e f o r m s s h o w that the r e l a t i o n -

plane of the n u c l e o l u s , since the p r o b a b i l i t y of not

ship b e t w e e n b o t h structures are v e r y close, and that

having s a m p l e d a C C - c o n t a i n i n g n e u r o n increases

the differences are d u e to interspecific causes. T h e first C C s d e v e l o p a r o u n d p o s t n a t a l day 30 and

with n e u r o n size.

40.

03 Z O i,i Z

A

30

20

20.

IO

I0.

O

0

IO

I0

2O

20 t

u.

0

40.

:30.

2~0

n-" 3O uJ 20 Z

D

4O

B

4O

20

IO

I0

IO

I0

0

20

2O ---/t . . . . . . .

9

II

13

,,-// . . . .

,

15

17

19

21

23

2,5

'27

NEURONAL

9 BODY

II

DIAMETER

13

15

17

tO

21

23

25

27

(}~m)

Fig. 4. Cell diameter histograms showing the size distribution of cells sampled at random, in the plane of the nucleolus, at each age. Filled squares: neuronal bodies which contain a CC; open squares: neuronal bodies without CC. A - D : 3-, 5.5-, 29- and 31-month-old rats, respectively.

236 increase steadily in n u m b e r during the next 4 months (Table II). A similar profile has been described in the postnatal d e v e l o p m e n t of the CLBs in the neurons of the cat L G N d 2°. It must be r e m a r k e d that the first CCs a p p e a r at the age of one m o n t h , the time at which the neurons of the L G N d of the rat have completed differentiation and achieved maturity 35'4°'43. Variations in the percentages of neurons with CCs were observed among the rats studied (Table II). Percentages of neurons of the L G N d of the cat containing CLBs given by different authors are also very variable: thus, while D o o l i n et al. 6 and G l a n z m a n et al II report that a r o u n d 10% of the neurons in the L G N d contain CLBs, Schmidt and Hirsch 45 give 39% and L e V a y and F e r s t e r 25 a r o u n d 45%. W h a t is more, H e r m a n and Ralston 18 have p o i n t e d out that while they had observed 46 neurons with CLBs in the ventrobasal and posterior thalamus of the cat, two-thirds of them were in one cat and 6 cats had none. The average percentage of neurons with two CCs has been found to be 1.82%. Percentages given by other authors are equally small; while Kalil and W o r den 2° r e p o r t that less than 5% of the CLB cells contained m o r e than one laminated body, Schmidt and Hirsch 45 give an average percentage of 0.3%; Herman and Ralston 18 describe that only once is m o r e than one body seen in an individual dendrite, and they thought that this may represent an i n t e r r u p t e d section through the same structure; as for Madarfisz et al. 29, they are the only ones who give a high percentage of neurons with two CLBs, since they r e p o r t 7 neurons out of 40 neurons studied. Ever since the study m a d e by L e V a y and F e r s t e r 25 in which they affirmed that the CLBs were found only in Guillery's type 2 cells and the X-cells in the cat L G N d , these little u n d e r s t o o d cytoplasmic organelles have b e c o m e specially interesting. A l t h o u g h the neuronal physiomorphological studies m a d e by F r i e d l a n d e r et al. 7 can be taken as indirect support for the L e V a y and Ferster 25 proposal that neurons with CLB are X-cells, they think that not all X-cells have this cytoplasmic structure. There exist, however, studies that have questioned this close relationship and which conclude that there is no clear correlation b e t w e e n CLB-containing and X- or class 2 cells of the cat L G N d 10"19'20~45. G l a n z m a n et al. 11 in their rabbit L G N d studies argue also against the L e V a y and F e r s t e r ' s hypothesis, since the rabbit L G N d does

not contain CLBs, and X-cells represent approximately 20% of the total population of geniculate neurons in the rabbit. The rat, being an animal in which pattern vision is of considerably little importance and no p r o m i n e n t area centralis is developed, has an X-system which is hard to detect ~5'49. In the rat only two functional channels within the retinogeniculate pathway have been described, which are now believed to correspond to the Y- and W-channels 8'9'15. The m o r p h o logical data of Kriebe122 and B r a u e r et al. 3 agree with these observations: that only a very small n u m b e r of cells in the lateral part resembles X-cells in some detail. O u r cell diameter histograms show a unimodal distribution of cell sizes both in the neuronal population which contains a CC in the plane of the nucleolus and in those which do not, at all ages (Fig. 4). This, together with the high percentage of CC-containing neurons (Fig. 1; Table II) makes the distribution of these cytoplasmic inclusions h o m o g e n e o u s in neurons of all sizes, except the smallest ones. This differs from what has been found by most authors 1°'2°'25 in the cat, since CLB-containing cells are a relatively restricted subset of m e d i u m size neurons. Therefore, given that in the L G N d of the rat the percentage of CC-containing neurons is high (Fig. 1 ; Table II) and that the distribution of this inclusion is h o m o g e n e o u s in neurons of all sizes except the smallest (Fig. 4) and also that the n u m b e r of X-cells, in case they exist, is very small 3'15'22 we conclude that CCs cannot serve as reliable morphological markers for L G N d X-cells in the rat. Although cell body size alone is not an a d e q u a t e criterion for distinguishing neuron types, the great majority of smaller neurons correspond, in all probability, to the interneurons ~2"22"53,which are G A B A e r gic 34 and which, as can be seen in Fig. 4, and as Lieberman 27 already proved, have no CCs. The same characteristics have been defined in the interneurons of the cat L G N d ; they are the smallest sized neurons, they are G A B A e r g i c cells and lack a laminar body25,26,29,46. Although the significance of these structures is still completely unknown, Madarfisz et al. 29 have suggested that CLBs might contribute to the survival of the neurons in the L G N d of the cat after decortication 5'17'5°, since almost all surviving P-cells have contained CLBs, whereas P-cells which do not possess

237 such organelles in the r a b b i t or m o n k e y L G N d 11'16'55 were described as d i s a p p e a r i n g c o m p l e t e l y after decortication 5'3°'31'36'37'42'44'51'52. H o w e v e r , the studies

might be e x p l a i n e d by a s s u m i n g differential sensitivity of cat relay cells or a x o t o m y .

a b o u t t r a n s n e u r o n a l r e t r o g r a d e d e g e n e r a t i o n in the rat L G N d which show a total d e p l e t i o n of n e u r o n s 4'z4

To s u m up: CCs in the L G N d of the rat are cytoplasmic inclusions with an u n k n o w n f u n c t i o n ; they are closely related to the CLBs of the cat a n d m o n -

a n d the data in the p r e s e n t study which show a high p e r c e n t a g e of n e u r o n s c o n t a i n i n g CCs, do n o t support Madarfisz et al.'s 29 p r o p o s a l in the rat, since CCs

key, a n d their origins are related to the e n d o p l a s m i c reticulum. T h e y a p p e a r once the n e u r o n has m a t u r e d a n d their n u m b e r increases progressively d u r i n g the

do n o t c o n t r i b u t e to the survival of g e n i c u l a t e n e u -

next 4 m o n t h s , a l t h o u g h their density is variable in all

rons after decortication. T h e discrepancy b e t w e e n the almost total d e p l e t i o n of n e u r o n s d u r i n g retrograde d e g e n e r a t i o n f o u n d in the L G N d of the rat 4'24, rabbit 5'3°, m o n k e y 31'51'52 a n d m a n 39, a n d , o n the oth-

the rats studied. T h e y are p r e s e n t in n e u r o n s of all sizes, except in the i n t e r n e u r o n s .

er h a n d , L G N d of the cat, in which m a n y n e u r o n s persist following d e s t r u c t i o n of visual cortex 5,29,

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