Neurons of the Dorsal Lateral Geniculate Nucleus of the Albino Rat R. M. KRIEBEL' Department of Anatomy, Medical College of Virginia, 12th & Broad Streets, Richmond, Virginia 23298

ABSTRACT Light and electron microscopic observations were made on the dorsal lateral geniculate nucleus (DLGN) of 33 young adult male albino rats. Three variants of the Golgi silver impregnation technique were employed in the light microscopic studies. Neurons were classified into three categories based on location, dendritic pattern, and dendritic appendages. Type 1 and type 3 neurons were distributed throughout the DLGN. Type 2 neurons were located in the superficial zone. Dendritic appendages of type 1 and type 2 neurons indicated these cells may function as geniculo-cortical relay neurons. The type 3 neurons had lobulated dendritic appendages and an axon that terminated within the nucleus. Type 3 neurons may represent Golgi-type I1 interneurons. Camera lucida drawings, photomicrographs, and electronmicrographs illustrate the characteristics of the three cell types. The literature on ultrastructural and neurophysiological findings may substantiate the presence of three neuronal types. Initially, the rat DLGN does not appear as elaborately organized as the nucleus observed in cats and primates; however, there are notable similarities in neuronal morphology and synaptology. The significance of subcortical synaptic interactions between neurons of the dorsal lateral geniculate nucleus and their role in vision has received considerable attention. Examination of the dorsal lateral geniculate nucleus (DLGN) has been pursued primarily in primates and carnivores, and excellent reviews of the DLGN of these species have appeared in the literature (Szentagothai et al., '66; Wiesel and Hubel, '66; Guillery, '71; Sanderson, '71; Kaas et al., '72; Famiglietti' and Peters, '72; Wong-Riley, '72). The present investigation examined the DLGN of yet another mammal, namely, the laboratory rat. The literature on the DLGN of the rat has been minimal compared to the anatomical and physiological studies in primates and cats. The reader is referred to the report of Grossman et al. ('73) for the most recent references related to the DLGN of the rat. In addition, Fukuda ('73) and Fukuda, Sugitani, and Iwama ('73) presented recent advances in unit activity recording from the neurons within the rat DLGN. Also, several authors have noted the use of the rat in J.

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visual behavior experimentation (Munn, '50; Silver, '67; Rosenberger and Ernst, '71). Rodents are of considerable interest in vision research for two primary reasons. First, it is known that species within the rodent order have a propensity to either a nocturnal or a diurnal existence. Further, it has been shown that these animals developed all-rod or all-cone retinas, respectively (Detwiler, '42; Walls, '42; Muntz, '67; Michael, '68; Jacobs and Yolton, '71). Second, differences in organization of the ipsilateral retinal projections have been demonstrated between pigmented and albino strains of rats (Sheridan, '65; Lund, '65; Adams and Forrester, '68; Guillery et al., '71; Cunningham and Lund, '71). The genetic explanation of the attendant albinism and misrouted retinogeniculate axons remains unknown. Ultrastructural characteristics of the rat DLGN were presented in the recent 1 Supported by U.S.P.H.S. Grant 5-T01-GM1410-05. This work was completed while R. Kriebel was a p r e doctoral candidate in the Department of Anatomy at Temple University School of Medicine, Philadelphia.

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reports of Lund and Cunningham ('72), Liberman and Webster ('72), and Liberman ('73). Routine electron microscopic preparations revealed detail of only an infinitesimal segment of a geniculate neuron and its synaptic relationships. Such ultrastructural information can often be supplemented by other morphologic techniques to obtain clearer understanding of geniculate function. For example, three dimensional appreciation of a geniculate neuron and its processes can be obtained by study of Golgi silver impregnation preparations (Colonnier, '64; Scheibel and Scheibel, '66, '70; Ramon-Moliner, '70; Chan-Palay and Palay, '72). The purpose of this investigation on the rat DLGN was to determine the neuronal cell types present and the morphologic characteristics of their dendrites and dendritic appendages which are distinguishable by Golgi impregnation. Recently, there has been interest in obtaining this basic information on the rodent DLGN from Golgi stained material (Kriebel, '73a; Grossman et al., '73; Rafols and Valverde. '73). It should be noted that Cajal ('11) discussed neuron types found in the DLGN of the rabbit and mouse. MATERIALS AND METHODS

and Palay ('72), the red impregnation reaction product was sought. Thus, impregnation time was relatively short with five days optimal for most diencephalic nuclei. The Golgi impregnated material was processed by either paraffin or frozen sectioning in transverse, parasagittal, and horizontal planes and at thicknesses of 25 p , 50 p , and 100 p. Frozen sectioning was preferred because it was fast and produced the least number of cracking artifacts. For mounting, the frozen sections were transferred directly from the knife to a pool of alcohol-gelatin (equal parts of 0.5% aqueous gelatin solution and 80% alcohol) on a glass slide. The sections were allowed to dry until the surface appeared "velvety". The slides were dipped in 95% alcohol and cleared in xylene. Cleared sections were enclosed in DiatexR and cover-slipped. Photographs of the Golgi impregnated tissue were taken with a Zeiss Ultraphot 111. All drawings were made with use of a Zeiss camera lucida attachment, a 10 x ocular, and 97 x oil immersion objective. Electron microscopic observations were made on seven rats. The ultrastructure of the DLGN of the rat was best preserved by gravity perfusion of a mixture of 4% paraformaldehyde and 0.5% glutaraldehyde (EM Sciences - pure glutaraldehyde) with 4% sucrose in 0.1 M phosphate buffer (pH 7.3). The precise location of the DLGN, as well as regions therein, was determined by a tissue-sampling method developed in our laboratory (Kriebel, '73b). Each specimen was processed routinely for EM and was carefully oriented as it was embedded in Epon. Thin sectioning was performed with the use of glass knives and a Sorvall PorterBlum MT2. The thin sections were stained for two minutes in uranyl acetate (Watson, '58) followed by five minutes in lead citrate (Venable and Coggeshall, '65). An RCA EMU-4 electron microscope operated at 50 Kv with a 25 micron objective aperture was used to examine the specimens of the DLGN.

The brains of 33 young adult male Holtzmann Sprague-Dawley albino rats were used in the present study. All animals ranged from 200-250 grams in body weight. All animals were anesthetized by an intraperitoneal injection of sodium pentobarbitol (dosage 50 mg/Kg). Gravity perfusion-fixation was completed through cannulation of the left ventricle of the heart. Three variants of the Golgi silver impregnation technique were employed as follows: four brains by the Golgi-Cox method (Jones, '50); two brains by the rapidGolgi method (Valverde, '70); and 20 brains by the Golgi-Kopsch technique (Romeis, '48; Colonnier, '74). The most detail of the dendritic appendages was observed in slides prepared by the GolgiKopsch method. The reliability of this techRESULTS nique, however, was enhanced by using Cajal's ('1 1) basic description of the small volumes of the 0.75% silver nitrate solution with several changes as recom- organization of the neurons in the rodent mended by Scheibel and Scheibel ('66). DLGN was readily verified in this study. Following the suggestion of Chan-Palay Some neurons were found lying adjacent

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to the inner border of the optic tract. The dendrites of these neurons usually coursed parallel to the fibers of the more superficial optic tract. However, some dendrites of these neurons projected deeper into the nucleus and were oriented perpendicular to the incoming optic fibers. Other neurons located deeper in the nucleus had dendrites which branched with no apparent orientation. In the present investigation, close examination of several hundred individual neurons revealed some distinguishing features. The neurons observed in the DLGN of young adult male albino rats used in this study could be classified into three types based on dendritic pattern and the arrangement of dendritic appendages.

populated with rounded protrusions that extended into the surrounding neuropil for short distances (arrows fig. 5). As illustrated by the camera lucida drawing in figure 2, many type 1 neurons showed the greatest number of rounded protrusions on the vertically directed dendrites. The horizontally oriented dendrites had a smoother contour and a reduced number of dendritic protrusions. Comparable short-stalked dendritic appendages were observed frequently in the electron microscope (fig. 6). In most instances these appendages appeared to be encased by large axon terminals containing round vesicles. It can be seen in figure 6 that such arrangements usually were surrounded by glial processes.

Type 1 neurons The type 1 neuron predominated and was observed throughout the DLGN. A type 1 neuron is identified by the arrow in figure 1. The perikarya were generally multipolar (mean diameter of 25 p ) giving off four to eight primary dendrites. A short distance from the cell body the primary dendrites branched and formed three to six secondary dendrites. The secondary dendrites again divided and formed a variable number of branches. This dendritic arrangement was termed the “tufted dendritic pattern” by Ramon-Moliner (’68) and is typical of most thalamocortical relay neurons (figs. 1 , 2). As shown by the neuron in figure 2 the dendritic processes were relatively straight and extended 108 p to 120 p into the neuropil. It should be noted in figure 1 that the dendrites of the type 1 neurons were primarily oriented perpendicular to the optic fibers coursing through the DLGN. A s shown in figure 3, the proximal portions of the primary dendrites of type 1 cells were smooth. Dendritic appendages appeared only after the primary dendrites had bifurcated. Typical of the type 1 neurons were short-stalked appendages with large terminal swellings 1.5 p in diameter (arrow in figs. 3, 4). The diameters of these terminals varied between 1.2 p and 1. 7 p. Some of the terminals had short thick stalks, whereas others had slightly longer and more slender stalks. The most distal dendrites were approximately 1 p in diameter and were heavily

Type 2 neurons Type 2 neurons were found only in the superficial zone of the middle third (anterior to posterior) of the DLGN (fig. 7). The cell bodies of these neurons had a mean diameter of 20 p. The dendrites of the type 2 cell were not observed to extend into the medial zone of the nucleus. The dendrites of these neurons were not as numerous and were shorter than those of the type 1 neuron. Also, the dendritic arborizations were observed to extend parallel to the optic fibers. An example of the type 2 neuron is indicated by the arrow in figure 7. In comparison to the primary dendrites of the type 1 neurons, the primary dendrites of the type 2 neurons extended further from the soma before bifurcating into secondary dendrites. The primary dendrites again had a smooth surface. The most characteristic feature of the type 2 neurons is indicated by the thick arrow in figure 8. At the bifurcation of the primary dendrites of the type 2 neurons a dense cluster of dendritic appendages was usually observed (figs. 7, 8, 9). The appendages within each of these clusters were characterized by either a spherical or ovoid enlargement 0.7 p to 1 p in diameter attached to the dendrite by a short stem (arrow in fig. 9). Smaller aggregations of appendages were also found on the secondary dendrites of the type 2 neurons (arrows in figs. 10, 11). The terminal rounded enlargements in these clusters had diam-

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eters that approximated 0.5 p. These terminals were somewhat smaller than those found in the larger more proximal clusters of dendritic appendages. Clusters on the secondary dendrites varied in configuration. Some appeared to have several rounded terminals arranged in a tight cluster and attached to the secondary dendrite by a common stem. An example of this type is indicated by the arrow in figure 10. Others had single rounded terminals attached to the parent dendrite by a single stem (fig. 11). Such terminals usually appeared in groups of two to four appendages. The distal dendrites of the type 2 neurons remain relatively smooth; however, rounded and finger-like protrusions were observed on the distal dendrites of the type 2 neurons. It should be noted that in the present investigation the origin and course of the axons from the type 1 and 2 neurons could not be identified. Ultrastructural study of the neuropil revealed many complex synaptic arrangements. Dendritic appendage clusters that resembled those characteristic of type 2 neurons participated in these synaptic configurations as shown in figure 12. Note that such appendages were surrounded by large axon terminals (RL in fig. 12). The parent dendrite,. the dendritic appendage, and the large axon terminals synapsing on the appendage were, in many cases, completely surrounded by glial lamellae. In this study these synaptic complexes were identified as “synaptic glomeruli” (Szentagothai, ’63) or “encapsulated zones” (Guillery, ’69) of the rat DLGN. Type 3 neurons Type 3 neurons were found in all regions of the DLGN. However, of the three neuronal types the type 3 neurons were least often identified. These neurons had small rounded perikarya (mean diameter of 14 p ) with relatively few dendrites. In some instances only primary dendrites were identified. The characteristic features of the type 3 neurons are well illustrated in figures 13 and 14. The dendrites extended from the soma in a “radiate dendritic pattern” (RamonMoliner, ’68). The dendrites had a tortuous course through the neuropil with no

apparent orientation to retinal or cortical afferents. Usually, no more than two or three branches were given off from one primary dendrite. The side branches were rarely observed to divide. The dendritic pattern reconstructed in figure 14 was one of the most complex observed on a type 3 neuron. The dendritic appendages provided the most characteristic feature of the type 3 neurons. The appendages had long pedicles that were 3 p to 6 p in length. The slender pedicles usually branched from the dendrites almost a t right angles (arrows in fig. 14). The primary pedicle of a n appendage at times gave rise to the side branches which ended in spherical or ellipsoid a1 enlargements that had diameters of 0.7 p to 1 p. Several variations of these dendritic appendages are identified by the arrows in figures 14 through 20. The two extremes of the characteristic neuronal type 3 dendritic appendages are illustrated in figure 20. Some stout appendages were attached to the dendrites by thick pedicles which then ended as club-shaped enlargements (arrow A in fig. 20). These appendages protruded from the dendrite into the neuropil for short distances (i,e., 2.5 p to 3 p ) . In contrast, other appendages had slender pedicles which pursued long tortuous courses through the neuropil. These slender pedicles often gave origin to side branches which terminated as lobulated enlargements (arrow B in fig. 20). In addition, the thin pedicles often demonstrated varicosities along their length. Such varicosities displayed a morphology that is similar to boutons en passant (B and arrowhead in fig. 20). In several instances, the thin axons of the type 3 neurons could be identified a s they arose from the perikarya or a proximal dendrite. The axons of these neurons usually ramified in the vicinity of the perikarya of origin (a in fig. 14). Type 3 neurons were usually impregnated in groups. Within groups of type 3 neurons the dendritic field of one neuron often overlapped the intervening dendritic processes of an adjacent type 3 neuron. Such a dendritic overlap is indicated by the thick arrow above the reconstructed neuron shown in figure 14.

NEURONS OF RAT DLGN-GOLGI DISCUSSION

Early in the present study, we were cognizant that neurons in the rat DLGN were similar to those described in the cat DLGN by Guillery (’66). Our classification of the neurons in the rat followed that proposed by Guillery (‘66) for the cat. Indeed, there were similarities between the three types of neurons identified in our Golgi preparations of the rat DLGN and the various types of DLGN neurons described in primates and cats. Such similarities between the geniculate neurons of rodents and other mammalian orders had not been reported prior to the reports by Kriebel (‘73a) and Grossman et al. (‘73). The type 1 neurons observed in the present study correspond to the class 1 cells described in the cat by Guillery (‘66). Our type 1 neurons also resembled the type I neurons identified by Wong-Riley (‘72) in the squirrel monkey. CampsOrtega et al. (’68) reported similar neurons in the macaque. It is worthy to note, that Lund (’70) and Lund and Cunningham (’72) referred to Golgi studies on the rat DLGN in two communications. These investigators stated that a single pear-shaped cell-type with four to five major dendrites predominated in the rat DLGN. This single cell-type probably corresponded to the type 1 neurons described in the present study. Cunningham and Lund (’71) described the laminar pattern of the rat DLGN and they observed that the dendrites of most neurons did not cross from one lamina to another (Lund and Cunningham, ’72). However, in the present study the long dendrites of the type 1 neurons appeared to cross laminar borders. This observation suggests that some neurons may receive retinal afferents from both the ipsilateral and contralateral retinas (Lund and Cunningham, ’72). The characteristic dendritic appendages of the type 1 neurons were short-stalked appendages with large terminal swellings. Such appendages appeared to be a major site of retinal axon termination. In this study EM profiles that resembled these appendages received synaptic contact from large axon terminals which contained round vesicles. The large axon terminals are presumably of retinal origin (Wong-

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Riley, ’72; Lund and Cunningham, ’72). Such axon terminals and dendritic appendages formed a component part of the synaptic glomeruli in the rat DLGN. It will be recalled that distal dendrites of the type 1 neurons were characterized by multiple rounded protrusions. These protrusions may provide a greater surface area for synaptic contact. Indeed, in our EM studies small terminals with round vesicles were observed to synapse on rounded protrusions as well as on the shaft of small dendritic profiles. Structurally, these terminal profiles resembled the SD terminals identified in the rat by Lund and Cunningham (’72). These authors stated that some of these terminals represented the cortico-geniculate input to the rat DLGN. The distal dendrites of the type 1 neurons probably do receive synapses from cortico-geniculate axons. Guillery (’69) observed that the distal dendrites of geniculo-cortical neurons of the cat received feed-back cortico-geniculate axon terminals. This concept has been supported by several investigators (Szentagothai, ’63; Szentagothai et al., ’66; Jones and Powell, ’69; Wong-Riley, ’72). The type 2 neurons in this study of the rat DLGN correspond to the class 2 neurons identified in the cat by Szentagothai (‘63) and Guillery (’66). This type of neuron was identified also in the primate DLGN by Campos-Ortega et al. (‘68) and by Wong-Riley (’72). In our study and preceding reports of different species the characteristic feature of the type 2 neuron was the clustered dendritic appendages at the point of bifurcation of the primary dendrites. Electron micrographs of the rat DLGN demonstrated profiles which appeared very similar to the dendritic appendages of the type 2 neuron. These appendages received multiple synaptic contacts from large axon terminals with round synaptic vesicles as shown in figure 12. In several studies similar clusters were identified as the primary components in the “synaptic glomeruli” of Szentagothai (‘63) or the “encapsulated zones” of Guillery (’69). The type 2 neurons may represent a more specialized neuron than the type 1 cell. In the primate, for example, WongRiley (’72) described a larger population

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of type I1 than type I neurons. The reverse was found in this study of the rat DLGN. The type 1 neurons were more plentiful and found in all regions of the rat DLGN. The type 2 neurons, on the other hand, were restricted to the superficial zone and were located predominantly in the middle region (anterior to posterior) of the nucleus. The limited dendritic field of the type 2 neurons could represent a more specific retinotopic input to this type of neuron. It should be recalled that class 2 neurons in the cat were identified only in laminae A and A1 of the cat DLGN (Guillery, ’66). Therefore, laminae A and A1 of the cat and the superficial zone of the rat DLGN possess similar types of neurons. This neuronal distribution is of particular interest inasmuch as the synaptology of these two regions is similar in rats and cats (Lund and Cunningham, ’72). Lund and Cunningham (‘72) and preliminary studies of the author revealed the synaptology was comparable to that described and illustrated in laminae A and Al by Guillery (‘69). The regions in both the cat and rat DLGN have an abundance of complex synaptic profiles often encapsulated by glial membranes. The class A cells described by Grossman et al. (’73) undoubtedly correspond with the type 1 and 2 neurons described and illustrated in the present study. We believe that type 1 and 2 neurons represent two varieties of geniculo-cortical relay neurons in the rat DLGN. This belief is based on neuronal size, location and characteristics of their dendritic appendages. There are further anatomical and physiological observations that support the concept of two distinct neuronal types. Anatomically, Lund and Cunningham (‘72) described “complex encapsulated synaptic zones” which occurred only in the superficial zone of the rat DLGN. These synaptic complexes received nonoverlapping crossed and uncrossed retinal projections. It is quite possible that the type 2 neurons provide the dendritic substrates of these “complex encapsulated synaptic zones.” Recent electrophysiological studies on unit activity in the rat DLGN are also of interest (Fukuda, ’73; Fukuda et al., ’73). These investigators divided the geniculo-

cortical neurons into two groups. According to their response latencies to optic nerve stimulation and light-flash stimulation, the principal or P cells were classified as either fast or slow neurons. A t this time available data does not permit specific correlation of the type 1 and 2 neurons with either the fast or slow P cells. The type 3 neurons identified in the rat DLGN possessed characteristics that resembled the class 3 cells of the cat (Guillery, ’66) and the type I11 neurons observed in monkeys (Wong-Riley, ’72). In the present study type 3 neurons had radiating dendrites, with long-pedicle appendages, and short axons that ramified in the vicinity of the neuron. Throughout the literature this type of neuron has been the candidate for the Golgi-type I1 cell, or interneuron in thalamic nuclei (Tello, ’04; OLeary, ’40; Polyak, ’57; Morest, ’64, ’65; Szentagothai et al., ’66; Guillery, ’66; Tombol, ’67, ’69; Ralston and Herman, ’69; Campos-Ortega et al., ’68; Famiglietti and Peters, ’72). The most interesting and characteristic feature of the type 3 neurons was the wide variety in structure of their dendritic appendages. In the cat DLGN, Famiglietti and Peters (’72) termed the bizarre dendritic appendages of the Golgi-type I1 neurons the “multi-lobed” appendages. These authors did an extensive study of thin serial sections through these appendages. Two significant points in their results should be mentioned in view of the resemblance between the dendritic appendages of the type 3 neurons in the rat and the “multi-lobed” appendages observed in the cat. First, the multi-lobed dendritic appendages possessed synaptic vesicles. The vesicles in these dendritic appendages were usually flattened. Second, they formed prominent components of the synaptic glomeruli in the cat DLGN. Basically, Famiglietti and Peters (’72) suggested that the Golgi-type I1 neurons functioned as internuncials between two or more synaptic glomeruli. Both the axons and dendrites of these cells participated in such interglomerular connections. Although ultrastructural profiles containing flattened synaptic vesicles have been observed in our studies, we have not been able to identify the parent neuron.

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It has been speculated that the inter- of this report. The author expresses sinneurons in the DLGN have an inhibitory cere appreciation to Nancy M. Kriebel for function (Singer and Crentzfeld, '70; her assistance in the preparation of the Szentagothai, '70; Kalil and Chase, '70; illustrations. Famiglietti and Peters, '72). The electroLITERATURE CITED physiological study of Burke and Sefton Adams, A. D., and J. M. Forrester 1968 T h e projection of the rat's visual field o n the c e r e ('66a,b) identified the presence of inhibibra1 cortex. Quart. J. Exp. Physiol., 53: 327-336. tory interneurons within the rat DLGN. W., and A. J. Seften 1966a Discharge The type 3 neurons which have been Burke, patterns of principal cells and interneurones in demonstrated in this study may represent lateral geniculate nucleus of rat. J. Physiol., 87: 201-212. the morphological counterpart of the cells 1966b Inhibitory mechanisms in lateral identified functionally by Burke and Sefton. geniculate nucleus of rat. J. Physiol., 187: 231It will be recalled that the axons of the 246. type 3 neurons ramified in the vicinity of Cajal, S. Ramon y 1911 Histologie du systeme nerveux d e l'homme et des vertebres. Norbert the neuron perikaryon. Some investigators Maloine, Paris, 2 vols. have further divided the Golgi-type I1 neuJ. A., P. Glees and V. Neuhoff rons of the cat on the basis of the axonal Campos-Ortega, 1968 Ultrastructural analysis of individual ramifications. For example, Tombol ('69) layers in the lateral geniculate body of the mondescribed both short and long-axon interkey. Z. Zellforsch., 87: 82-100. neurons in the cat DLGN. The functional Chan-Palay, V., and S. L. Palay 1972 High voltage electron microscopy of rapid Golgi prepsignificance of these two types of interarations. Neurons and their processes in the neurons is not understood, cerebellar cortex of monkey and rat. Z. Anat. The description of type 3 neurons in Entwick1.-Geseh., 137: 1 2 S 1 5 2 . the present study conforms with that of Colonnier, M. 1964 The tangential organization of the visual cortex. J. Anat. (London), 98: the class B cells shown by Grossman et al. 327-344. ('73). These authors reported that some Cunningham, T. J., and R. D. Lund 1971 LamClass B cells did not possess an axon. We inar patterns in the dorsal division of the lateral geniculate nucleus of the rat. Brain Res., 34: have also observed cells of this nature 394-398. which did not demonstrate any recogniza- Detwiler, S. R. 1943 Vertibrate Photoreceptors. ble axon and attributed this to a lack of Macmillan, New York. impregnation. However, it has been sug- Famiglietti, E., and A. Peters 1972 The synaptic glomerulus a n d the intrinsic neuron in gested that some DLGN neurons are withthe dorsal lateral geniculate nucleus of the cat. out axons (i.e., anaxonal) (LeVay, '71; J. Comp. Neur., 144: 285-334. Wong-Riley, '72; Scheibel et al., '72; Lie- Fukuda, Y. 1973 Differentiation of principle berman, '73). cells of the r a t lateral geniculate body into two groups: Fast a n d slow cells. Exp. Brain Res., Initial inspection indicated that the rat 17: 242-260. DLGN was not as elaborately organized Fukuda, Y., M. Sugitani and K. Iwama 1973 as the nucleus observed in other animals. Flash-evoked responses of two types of principal However, the rat nucleus does possess cells of the rat lateral geniculate body. Brain Res., 57: 208-212. both neuronal features and a synaptology comparable in many respects to those Grossman, A,, A. R. Lieberman and K. E. Webster 1973 A Golgi study of the rat dorsal lateral which have been described by others for geniculate nucleus. J. Comp. Neur., 150: 441the DLGN in primates and cats. Although 466. only limited attention has been given to Guillery, R. W. 1966 A study of Golgi preparations from t h e dorsal lateral geniculate nucleus the anatomy of the rodent visual system, of the adult cat. J. Comp. Neur., 128: 21-50. there are many challenges in basic visual 1969 T h e organization of synaptic inresearch to be pursued in these animals. terconnection in the laminae of the dorsal latACKNOWLEDGMENTS

I wish to extend my thanks to Dr. Raymond C. Truex for his support and advice throughout this study and in preparing this manuscript. In addition, the author thanks Dr. W. P. Jollie and Dr. H. R. Seibe1 for their careful and critical reading

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Thesis: Temple University, Philadelphia. geniculate nucleus of the cat. Brain Res., 1 3 : 159-177. LeVay, S . 1971 On the neurons and synapses of the lateral geniculate nucleus of the monkey, Scheibel, M. E., and A. B. Scheibel 1966 T h e and the effects of eye enucleation. Z. Zellforsch., organization of the nucleus reticularis thalami: 113: 3 9 6 4 1 9 . A Golgi study. Brain Res., 1 : 43-62. Lieberman, A. R. 1973 Neurons with presyn1970 The rapid Golgi method. Indian aptic periparya and presynaptic dendrites in summer or Renaissance? I n : Contemporary the rat lateral geniculate nucleus. Brain Res., Research Methods in Neuroanatomy. W. J . H. 5 9 : 35-59. Nauta and S . 0. E. Ebbesson, eds. SpringerLieberman, A. R., and K. E. Webster 1972 PreVerlag, New York, pp. 1-11. synaptic dendrites and a distinctive class of synScheibel, M. E., T. C. Davies and A. B. Scheibel aptic vesicle in t h e rat dorsal lateral geniculate 1972 An unusual axonless cell in the thalamus nucleus. Brain Res., 4 2 ; 1 9 C 2 0 0 . of the adult cat. Exp. Neur., 3 5 : 512-518. Sheridan, C. L. 1965 Interocular transfer of Lund, R. D. 1965 Uncrossed visual pathways brightness and pattern discrimination in norof hooded and albino rats. Science, 1 4 9 : 1506mal and corpus Callosum-sectioned rats. J. 1507. Comp. Physiol. Psychol., 5 9 : 292-294. 1970 Structural organization of the Silver, P. H. 1967 Spectral sensitivity of the superior colliculus and dorsal lateral geniculate white r a t by a training method. Vision Res., body of the rat. J . Physiol. SOC.Jap., 32: 5557 : 377-383. 556. Singer, W., and 0. Creutzfeldt 1970 Reciprocal Lund, R. D., and T. J. Cunningham 1972 Aslateral inhibition of on- and off-center neurons pects of synaptic and laminar organization of in the lateral geniculate body of the cat. Exp. the mammalian lateral geniculate body. Invest. Brain. Res., 10: 311-330. Ophthalmology, 1 I : 291-302. Szentagothai, J . 1963 The structure of the synMichael, C. R. 1968 Receptive fields of single apse in the lateral geniculate body. Acta. Anat., optic nerve fibers in a m a m m a l with an all5 5 : 166-185. cone retina. I. Contrast-sensitive units. J. 1970 Gomerular synapses, complex Neurophysiol., 31 : 249-256. synaptic arrangements, and their operational Morest, D. K. 1964 The neuronal architecture significance. In: The Neuroscience: A Second of the medial geniculate body of the cat. J . Anat. Study Program. F. Schmitt, ed. The Rockefeller (London), 9 8 : 61 1 4 3 0 . University Press, New York, pp. 4 2 7 4 4 3 . 1965 T h e lateral tegmental system of the midbrain and the medial geniculate body: Szentagothai, J., J . Hamon and T. Tombol 1966 a study with Nauta and Golgi methods in cat. Degeneration and electron microscopy analysis J . Anat. (London), 99: 611-634. of the synaptic glomeruli in the geniculate body. Munn, N. L. 1950 Handbook of Psychological Exp. Brain Res., 2: 283-301. Research on the Rat; An Introduction to AniTello, F. 1904 Disposicion macroscepica y m a l Psychology. Houghton Mif€lin, Boston. estructura del cuerpo geniculado externo. Trab. Muntz, W. R. A. 1967 A behavioral study on Lab. Invest. Biol. Univ. Madrid, 3 : 3 9 4 2 . photopic and scotopic vision in the hooded rat. Tombol, T. 1967 Short neurons and their synVision Res., 7 : 371-376. aptic relations in the specific thalamic nuclei. O’Leary, J. L. 1940 A structural analysis of the Brain Res., 3: 307-326. lateral geniculate nucleus of the cat. J. Comp. 1969 Two types of short axon (Golgi Neur., 7 3 : 4 0 5 4 3 0 . 2nd) interneurons in t h e specific thalamic nuPolyak, S. 1957 The Vertebrate Visual System. clei. Acta. Morph. Acad. Sci. Hung., 1 7 : 285H. Kluver, ed. Univ. of Chicago Press, Chicago, 297. I

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NEURONS OF RAT DLGN-GOLGI Valverde, F. 1970 The Golgi method. A tool for comparative structural analyses. In: Contemporary Research Methods in Neuroanatomy. W. J. H. Nauta and S. 0. E. Ebbesson, eds. Springer-Verlag, New York, pp. 12-31. Venable, J. H., and R. Coggeshall 1965 A simplified lead citrate stain for use in electron microscopy. J. Cell Biol., 25: 4071108. Walls, G. L. 1942 The Vertebrate Eye. Bloomfield Hills, Michigan: Cranbrook Institute of Science.

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Watson, M. L. 1958 Staining of tissue sections for electron microscopy with heavy metals. J. Biophys. Biochem. Cytol., 4: 47-78. Wiesel, T. N., and D. H. Hubel 1966 Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J. Neurophysiol., 29: 1115-1156. Wong-Riley, M. T. T. 1972 Neuronal and synaptic organization of the normal dorsal lateral geniculate nucleus of the squirrel monkey Saimiri sciureus. J. Comp. Neur., 1 4 4 : 25-60.

PLATE 1 EXPLANATION OF FIGURES

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1

A coronal section through the middle region of the DLGN. Type 1 neuron indicated by arrow i s reconstructed in figure 2. Optic tract (OT), Hippocampus (H), Dorsal (D), Lateral (L). Golgi-Kopsch. X 102.

2

Camera lucida drawing of a type 1 neuron. Notice the tufted dendritic pattern. Two typical dendritic appendages of the type 1 neuron are shown near the cell body. The vertically directed dendritic tuft is studded with rounded protrusions (arrow). The location of the appendages shown i n figures 3 , 4 and 5 are indicated.

N E U R O N S OF RAT DLGN-GOLGI R. M. Kriebel

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PLATE 1

3

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PLATE 2 EXPLANATION O F FIGURES

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3, 4

Photomicrographs of a type 1 neuron. Notice the short-stalked dendritic appendages with large terminal swellings (arrows). GolgiKopsch. Figure 3, X 1,300;figure 4, x 2,200.

5

Distal dendrite of type 1 neuron. Note the rounded protrusions typical of the distal dendrites (arrows). Golgi-Kopsch. x 1,800.

6

Large axon terminal with round vesicles (RL) surrounds a shortstalked appendage (Da). This type of appendage appears to be similar to the characteristic appendages of the type 1 neurons observed in Golgi preparations (fig. 3). T h e profile of a terminal containing flattened vesicles (F) is shown indenting the periphery of the RL terminal. Note the glial processes (arrowheads) that surround the complex. X 29,700.

N E U R O N S OF RAT D L G N - GOLGI STUDY R. M. Kriebel

PLATE 2

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PLATE 3 EXPLANATION OF FIGURES

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7

Type 2 neuron indicated by thick arrow. This neuron is reconstructed in figure 8 . The optic tract (OT), dorsal (D), and lateral (L) are indicated for orientation. Golgi-Kopsch. X 300.

8

Camera lucida drawing of a type 2 neuron. A dense cluster of appendages (thick arrow) is seen at the point of bifurcation of a primary dendrite. The location of the dendritic appendages shown in figures 9, 10 and 11 are indicated.

N E U R O N S OF RAT DLGN R. M. Kriebel

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PLATE 3

10

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PLATE 4 EXPLANATION O F F I G U R E S

Figs. 9-11. karyia (NP).

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Dendritic appendages of a type 2 neuron. Neuron Peri-

9

Photomicrograph of dendritic appendages at the bifurcation of the primary dendrite. Arrow indicates a component of the cluster with a thick dendritic extension that terminated in a rounded enlargement. Golgi-Kopsch. X 2,100.

10

A small cluster of appendages on a secondary dendrite. Note several rounded enlargements (arrow) attached to the dendrite by a common pedicle (not shown in photograph). Golgi-Kopsch. X 2,100.

11

Dendritic appendages that appear as simple rounded expansions attached to the secondary dendrite by individual pedicles. GolgiKopsch. X 2,100.

N E U R O N S OF RAT DLGN - GOLGI STUDY R. M. Kriebel

PLATE 4

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PLATE 5 EXPLANATION OF FIGURE

12

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A dendritic appendage (Da) similar to those observed on type 2 neurons that receives synaptic contact (arrows) from large axon terminals with round vesicles (RL). Glial lamellae (arrowheads) encapsulate the appendage and vesicle containing profiles, as well as, the dendritic shaft. Note the numerous small unmyelinated s o n s (a) in this field. x 27,700.

NEURONS OF RAT DLGN - GOLGI STUDY R. M. Kriebel

PLATE 5

I

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PLATE 6 EXPLANATION OF F I G U R E S

13

Golgi-Kopsch preparation of rat DLGN in coronal section. Arrow in center indicates type 3 neuron that was reconstructed and is shown infigure14. X 270.

14

Camera lucida drawing of type 3 neuron. Note radiating pattern of dendrites. The small axon ramifying in vicinity of the cell body is identified (a). Thick arrow indicates dendritic overlap of an adjacent type 3 neuron. The location of the appendages illustrated in figures 15, 16 and 17 are indicated.

Figs. 15-17. Kopsch.

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Dendritic appendages (arrows) of a type 3 neuron. Golgi-

15

Long, thick pedicle that expanded into an irregular and blunted terminal. X 1,350.

16

Short, thin pedicle that terminated in a rounded swelling.

17

Long, thin pedicle which branched and terminated in multiple enlargements. X 1,350.

X

1,350.

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PLATE 7 EXPLANATION OF F I G U R E S

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18

Type 3 neuron. Note the long, slender pedicles with spheroid and ellipsoid terminal enlargements (arrows). Golgi-Kopsch. X 2,000.

19

Two characteristic dendritic appendages of the type 3 neuron (arrows). The attachment of the lobulated terminal to the dendrite is clearly shown (arrow 1). Golgi-Kopsch. X 710.

20

Two extremes of the dendritic appendages of type 3 neurons. Some appendages have thick, stout pedicles which expand into club-shaped terminals (A). Others have long slender pedicles ending in multiple lobulated enlargements (B). The swelling along appendage B has a morphology similar to a bouton en pas s ant (thick arrow). GolgiKopsch. x 2,800.

NEURONS OF RAT DLGN-GOLGI R. M. Kriebel

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Neurons of the dorsal lateral geniculate nucleus of the albino rat.

Neurons of the Dorsal Lateral Geniculate Nucleus of the Albino Rat R. M. KRIEBEL' Department of Anatomy, Medical College of Virginia, 12th & Broad Str...
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