* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download The projection of the lateral geniculate nucleus to area 17 of the rat
Multielectrode array wikipedia , lookup
Neuroeconomics wikipedia , lookup
Cortical cooling wikipedia , lookup
Action potential wikipedia , lookup
Long-term depression wikipedia , lookup
Single-unit recording wikipedia , lookup
Aging brain wikipedia , lookup
Premovement neuronal activity wikipedia , lookup
Optogenetics wikipedia , lookup
Eyeblink conditioning wikipedia , lookup
Neuropsychopharmacology wikipedia , lookup
Neuroregeneration wikipedia , lookup
Biological neuron model wikipedia , lookup
Environmental enrichment wikipedia , lookup
Neuromuscular junction wikipedia , lookup
Development of the nervous system wikipedia , lookup
End-plate potential wikipedia , lookup
Node of Ranvier wikipedia , lookup
Neuroanatomy wikipedia , lookup
Anatomy of the cerebellum wikipedia , lookup
Stimulus (physiology) wikipedia , lookup
Neurotransmitter wikipedia , lookup
Molecular neuroscience wikipedia , lookup
Dendritic spine wikipedia , lookup
Axon guidance wikipedia , lookup
Holonomic brain theory wikipedia , lookup
Activity-dependent plasticity wikipedia , lookup
Feature detection (nervous system) wikipedia , lookup
Nervous system network models wikipedia , lookup
Nonsynaptic plasticity wikipedia , lookup
Synaptic gating wikipedia , lookup
Apical dendrite wikipedia , lookup
Chemical synapse wikipedia , lookup
Journal of Neurocytology 5, 85-Io7 (I976) The projection of the lateral geniculate nucleus to area I7 of the rat cerebral cortex. II. Terminations upon neuronal perikarya and dendritic shafts A L A N PETERS, M A R T I N F E L D M A N and J U L I A N S A L D A N H A Department of Anatomy, Boston University School of Medicine, Boston, Mass. 02118 U.S.A. Received 18 July I975; revised 17 September I975. accepted 25 September r 975 Summary The forms of dendrites in layer IV receiving degenerating thalamocortical axon terminals directly on their shafts were examined in serial thin sections. Reconstructions showed these dendrites varied in thickness between 2.5 and 0.5 [zm. They had essentially smooth contours and rarely showed evidence of protrusions or spines. They were further characterized by the presence of many synapses along their shafts. Only about one in I2 of these synapses was formed by degenerating thalamocortical axon terminals. These smooth dendrites emerged from neuronal perikarya that also received degenerating axon terminals which formed asymmetric synaptic junctions. Such cell bodies bore both symmetric and asymmetric synaptic junctions, and not all of the latter were caused to degenerate after a thalamic lesion. These postsynaptic neurons appeared to be of two kinds, ones with thin dendrites that often contained closely packed microtubules, and others with thicker dendrites that emerged from the poles of oval perikarya. Introduction To study the projections from the lateral geniculate nucleus to the cerebral cortex of the rat Ribak and Peters (I975) injected radioactive proline into the thalamus. They found that the dorsal portion of the lateral genicutate nucleus projects to the visual cortex and thereby confirmed the results of earlier anatomical studies by Clark (i932), Lashley (I934, I94I) and Waller (I934). In the cerebral cortex the disposition of the transported proline was largely confined to area 17 (Krieg, i946), although it extended to the zones of transition between area 17 and the peristriate areas I8 and I8a. In area 17 the radioactivity showed a major peak of labelling, and hence a primary site of termination of geniculocortical afferents, to be in 9 I976 Chapman and Hall Ltd. Printed in Great Britain 86 PETERS, FELDMAN and SALDANHA layer I V and lower layer I I I , with secondary sites of axon termination in layers I and VI. A similar distribution of geniculocortical afferents was also found by Rosenquist, Edwards and Palmer (I 974) in the cat. T h e s e observations on the rat were largely confirmed by a study in which lesions were placed in the lateral geniculate nucleus and the disposition o f degenerating axon terminals in the cerebral cortex determined by light and electron microscopy. I n this study (Peters and Feldman, 1976) it was shown that such lesions result in p r o m i n e n t degeneration of axon terminals in layer I V and lower layer I I I o f area 17, together with a sparse terminal degeneration in layers I and VI. Little terminal degeneration was apparent in u p p e r layer VI, although small degenerating myelinated axons occurred frequently and it was considered that these axons probably accounted for the elevated grain count in the radioactive proline study cited above. Such observations are essentially in agreement with those of other authors who have examined the projections of the lateral geniculate nucleus to the visual cortex in the cat and m o n k e y (e.g., H u b e l and Wiesel, 1962, 1972; Colonnier and Rossignol, 1969; G a r e y and Powell, 1971 ; Polley, 1971 ; Wiesel, H u b e l and Lain, 1974; Rosenquist, Edwards and Palmer, I974), and in the opossum (Benevento, 1972). I n the rat it has been shown that 15% of the degenerating geniculocortical axon terminals in layer I V f o r m synapses with dendritic shafts and 2 % with neuronal perikarya (Peters and Feldman, 1976). I n the present article the forms of the neurons receiving geniculocortical afferents on their shafts and perikarya are considered. T h e forms of the dendrites have been reconstructed through the use of serial thin sections examined in the electron microscope. Fig. I. Two dendrites (den1 and den2) forming asymmetric synapses (-+ s) with the same degenerating axon terminal (d). These dendrites also make synapses with normal axon terminals (At). Compared with the asymmetric synapses involving dendritic spines (sp) those on dendritic shafts have a less prominent postsynaptic density. These dendritic shafts have smooth contours and their cytoplasm contains many microtubules (m). Note the swelling of one of the mitochondria (mit) in the dendrite (denO on the left. • 3oooo. Fig. 2. A large dendrite (den) which forms synaptic junctions with one degenerating (d) and two normal (At) axon terminals. The dendrite has a smooth outline and its cytoplasm contains microtubules (m), polyribosomes (r), and a cistern of endoplasmic reticulum (ER). One mitochondrion (mit) shows a dilatation of its outer membrane. The degenerating axon terminal is surrounded by astrocytic processes (As) and it also synapses with a dendritic spine (sp). • 38ooo. Figs. 3 and 4. In Fig. 3 is a reconstructed dendrite with a shaft that bifurcates to form two thinner branches (I and 2). The left branch (1) receives a degenerating axon terminal ( 4 ) . All other synapses (stippling) are formed by normal terminals and with one exception which is symmetric ( 1~ ) the other junctions are asymmetric in form. Bar represents i ~m. The cytological appearance of the left hand branch (1) at the site where it receives the degenerating axon terminal (d) is shown in Fig. 4A. In (B), both branches are illustrated. The one on the right (2) forms a small spine (sp) at this location, while the other branch (1) receives two normal terminal~ (At). In (C), the left branch is quite thin and the thicker right branch receives two terminals (At). (D) illustrates the common shaft (den) which at this level is forming synapses with two terminals. The orientation arrows in this and subsequent reconstructions are explained in the text. Magnification of Fig. 4 is • 25000. I / / ! / J / / / 9~ PETERS~ FELDMAN a n d SALDANHA Material and m e t h o d s The data upon which this study is based are derived from a series of Sprague-Dawley rats, three months of age. Following placement of lesions in the lateral geniculate nucleus the animals were allowed to survive for periods of 2-4 days. They were then perfused through their vascular systems with solutions containing aldehydes and pieces of their visual cortex prepared for electron microscopy. Details of the lesions and the methods of preparation are given in the preceding article (Peters and Feldman, z976 ). To reconstruct the forms of the dendrites receiving degenerating and synapsing geniculocortical afferents on their shafts, serial thin sections through layer IV of the visual cortex were prepared. The material used for serial sectioning was obtained from the animal designated earlier (Peters and Feldman, I976 ) as animal L zo7. This animal was allowed to survive for four days after making the lesions which were confined to a small portion of the dorsal lateral genlculate nucleus. To prepare the thin sections blocks of plastic embedded cerebral cortex containing degenerating axon terminals were mounted so that they could be sectioned in a tangential plane; that is, parallel to the pial surface. After layers I through I I I had been removed sectioning was continued until layer IV was reached. The block face was then trimmed to a trapezoid about o.~ • o.2 m m in size and serial thin sections were taken. The sections were faintly golden in colour. These serial sections were collected onto Formvar coated grids with o.4 x 2 m m slots (Pelco) by using techniques described previously (Vaughan and Peters, z973). The series examined were up to I4o sections long. Once a dendritic shaft forming a synaptic junction with a degenerating axon terminal had been located, that dendrite was traced throughout the series and photographed, most commonly at a primary magnification of x 7500. The resulting photographic prints were xerox copied. On these copies the dendrite was marked in coloured pencil and all of the synaptic junctions along its length were identified. Reconstructions of the dendrite were made by using tracing paper upon which the outlines of successive profiles of the dendrite were drawn. The sequential profiles as they appeared in successive photographs were 'slipped', or overlapped by a constant amount proportional to the average thickness of each of the sections in the series. At the same time the orientation, or direction of passage of the dendrite relative to the plane normal to the pial surface of the cortex, was determined. This orientation, which can only be approximate, was largely determined by comparing the orientation of the dendrite with that of other components of the neuropil, especially the apical dendrites of layer V pyramidal neurons and the initial segments of axons of layer I I I pyramidal neurons, which are known to pass in an essentially normal direction with respect to the cortical surface. Results Appearanceof degeneration As a consequence of a lesion in the lateral geniculate body some of the axon terminals in layer IV of the visual cortex darken and undergo changes described in our previous article (Peters and Feldman, t976). Like all of the geniculocortical axon terminals undergoing Fig. 5- On the left are reconstructions of two dendrites (1 and 2). Dendrite 1 forms an asymmetric synapse with a degenerating terminal which also synapses with a dendritic spine (B). The shaft of this dendrite forms synapses (stippling) with other, and normal, axon terminals and only one of these ( 9 ) has a symmetric form. At the upper end of this dendrite (A) there is a lateral protrusion that resembles a spine and synapses with a normal axon terminal (At). Bar represents I ~m. Dendrite 2 also has a single degenerating axon terminal synapsing with its shaft (C). Micrographs x i9ooo. X I 92 PETERS, FELDMAN and SALDANHA degenerative changes, those forming synapses with the shafts of dendrites display asymmetric (Colonnier, I968), or type I (Gray, 1959) synaptic junctions. Such synapfic junctions are characterized by the presence of a relatively wide synaptic cleft (about 3~ and by a deposition of dense material on the cytoplasmic face of the postsynaptic membrane. It should be emphasized that specific reference is being made to the synaptic junction because in our material all of the synaptic vesicles appear to be spherical. Hence it is not possible to use vesicle shape as an added criterion for distinguishing between types of synapses (e.g. Colonnier, 1968). When the asymmetric synaptic junctions on the dendritic shafts are compared with those involving dendritic spines it becomes apparent that the density associated with the postsynaptic membrane of the dendritic shaft is less prominent (Fig. I). The reason for this seems to be that the cytoplasm of the dendritic spines contain a good deal of microfilameIztous, flocculent material that may become associated with, or incorporated into the postsynaptic density. This absence of a prominent postsynaptic density at synapses involving dendritic shafts can sometimes make the presence of a synaptic junction formed by a degenerating axon terminal difficult to recognize at low magnifications. Furthermore, there is sometimes uncertainty even at higher magnifications about the existence of a synaptic junction between a darkened axon terminal and a dendritic shaft. This is especially true when the plane of section is not exactly normal to the plasma membranes of a suspected synaptic junction. The same problem also pertains to the identification of synaptic junctions between degenerating axon terminals and neuronal perikarya. The dendrites receiving degenerating axon terminals along their shafts range in size from about 0.5-2.5 ~zm. In individual thin sections (Figs. I and 2) the postsynaptic dendrites have essentially smooth contours and their cytoplasm may have a rather closely packed array of microtubules. Cisternae of endoplasmic reticulum are frequently present and in the cytoplasm of the larger dendritic profiles, it is not uncommon to discern clusters of ribosomes, some forming polyribosomes, lying free in the cytoplasm and others attached to the surface of narrow cisternae. The mitochondria of these dendrites may be relatively large (mit) and at the level of the synaptic junction formed with a degenerating axon terminal it is not uncommon to find some distortion of one or more mitochondria. This distortion may take various forms, but as seen in Figs. I and 2, it is usually produced by a swelling or extension of the space between the inner and outer mitochondrial membranes. Such a swelling is not common at other levels of these dendrites. The profiles of the postsynaptic dendrites receiving degenerating axon terminals on their shafts frequently show normal terminals (Figs. I and 2) forming synapses at other locations on their circumference. The number of such synapses seen in a given section of a dendrite increases with the diameter of the profile. At the synapses with normal axon terminals the Fig. 6. On the left is the reconstruction of a dendrite with a rather even diameter. As indicated by the dashed lines, a part of this dendrite was omitted from the photographic series. However, as shown in the micrographs this dendrite could be recognized by its characteristic features of smooth contours and a close packing of the microtubules. Micrograph (B) shows this dendrite synapsing with the degenerating axon terminal. Bar in line illustration represents I ~m. Micrographs • 30000. r I ! 94 PETERS, FELDMAN and SALDANHA junctions are convex towards the axon terminals, and the outline of the dendrite is not appreciably altered by their presence. In contrast, synaptic junctions formed by the degenerating axon terminals are often concave, so that the surface of the dendrite is dimpled (Figs. I and 4A). Because this change in the configuration of the synaptic junction is so commonly encountered, it can only be assumed that it is related to an altering dynamic relationship between the degenerating axon terminal and its postsynaptic dendrite. While it is most common in single thin sections to find a degenerating axon terminal forming a synapse with only the shaft of a dendrite, examples have been encountered in which the same terminal also forms a second synaptic junction. This second junction can involve either another dendritic shaft (Fig. I), or a dendritic spine (Fig. 2 and Fig. 5B). Reconstructed dendrites The essentially smooth contours of these dendrites receiving degenerating geniculocortical afferents on their shafts becomes more apparent when their forms are reconstructed from serial thin sections, as shown in Figs. 3-7. At this point it will help to give an indication of how to interpret the five reconstructions illustrated here. As shown from the I ~m markers, the reconstructed lengths of the dendrites range from about 12-6 ~m. The thickest, 2.5 ~zm, is the common shaft shown in Fig. 3 and illustrated in Fig. 4D, while the thinnest is the narrow portion of dendrite I in Fig. 5 and illustrated in Figs. 5B and C. This is only o.5 ~m thick. In the reconstructions the positions of the degenerating axon terminals are indicated by arrows and represented by solid black areas. The locations of synaptic junctions formed by normal and undegenerating axon terminals are shown by stippling. The heavy stippling indicates that the synaptic junction is on the front face of the dendrite, and the lighter stippling that is on the back side. Accompanying each drawing is a symbol indicating the orientation of the dendrite. The thin line passing vertically and ending in an arrowhead indicates the direction of the pia mater, or the vertical plane of the cerebral cortex, while the thin horizontal line at right angles gives the tangential, or horizontal plane. The third and thicker line indicates the orientation in which the reconstructed dendrite lies with reference to these two planes. Lastly, the profiles of the dendrites reconstructed in Figs. 3, 5 and 6 as they appear at various places in the series are shown in accompanying electron micrographs, and the positions of these micrographs in the reconstructions are indicated by the lines whose letters correspond to those of the accompanying micrographs. The reconstructed dendrite illustrated in Fig. 3 is quite thick and the main dendritic shaft (Fig. 4D, den), which is presumably close to the neuronal perikaryon, gives rise to two branches (i and 2), each thinner than the main shaft. This reconstructed length of dendrite has some 34 synaptic junctions. Only one of these is formed by a degenerating axon terminal (Fig. 4 A, d). Furthermore with the exception of one normal synaptic junction which has a symmetric form (Fig. 3, ]~ ), all of the other unaltered synaptic junctions are asymmetric. Although most of the dendritic surface is smooth there are two small spines emanating from the right hand branch (2). One of these is illustrated in Fig. 4 B (sp) which shows the spine to be small, quite short, and to form only a tiny synaptic junction. The two reconstructed dendrites in Fig. 5 are thinner. Again they have relatively smooth contours and have a number of synapses along their shafts. As in the previous example each Geniculo-cortical projection in rats. II 95 Fig. 7- Reconstruction of the end of a smooth dendrite. This portion of the dendrite received two degenerating axon terminals (-~ s). Because of the oblique path of this dendrite relative to the plane of the serial sections no micrographs are shown, for they do not help in appreciating its cytological features. Bar represents I ~m. of these two dendritic segments receives only one degenerating axon terminal, and with the exception of a single synaptic junction at the bottom of dendrite I (l~), the normal synapses are asymmetric in form. While dendrite 2 has a relatively uniform thickness of about 1 9.m the surprising feature of dendrite I is the very thin middle segment. In this segment, including the place where it receives the degenerating geniculocortical axon terminal, the diameter of the dendrite is only about o.5 ~tm (Fig. 5B and C). This is much thinner than generally assumed for dendrites, and approaches the o.I--o. 3 ~zm range of most unmyelinated axons in the cerebral cortex. Indeed a dendritic profile of this form could easily be taken to be an unmyelinated axon since ribosomes in the cytoplasm are only sparse, and like axons, the main organelles are microtubules and mitochondria. Similar small dendritic profiles have 96 PETERS, FELDMAN and SALDANHA previously been encountered in layer I of the rat parietal cortex (Vaughan and Peters, 1973), and in both layer I and layer IV these are located between bulbous portions. Such a bulbous portion seems to be forming at the bottom of dendrite I. At this site the cytoplasmic organelles become somewhat dispersed as though the dendrite has become swollen. At the upper end of dendrite I in the reconstruction shown in Fig. 5 a lateral protrusion arises (Fig. 5A). This protrusion has the features of a dendritic spine, in that it receives an asymmetric synapse and the cytoplasm contains a flocculent assembly ofmicrofilaments. Like the dendrites described above, that illustrated in the reconstruction of Fig. 6 passes in a vertical direction through the neuropil. Unfortunately, as indicated by the dashed lines and the break in the reconstruction, this dendrite was omitted from several of the photographs of the series. However, some of the components of the neuropil could be sufficiently well identified for the reconstruction to be continued beyond the break. In addition, this dendrite has such characteristic features that it stands out from other dendrites in the field (Fig. 6A-C). These features are the smooth and rounded contours of the profiles, the presence of asymmetric synapses on the dendritic shaft, and the close packing of microtubules in the cytoplasm. As in other examples, only one synapsing axon terminal is degenerating (Fig. 6B). The remaining synapsing axon terminals (At) are normal. The last reconstructed dendrite is shown in Fig. 7- This differs from the previous ones in two important ways. First, this length of dendrite receives two degenerating axon terminals (-~s), although there are sixteen other synaptic junctions along its shaft which are formed by normal axon terminals. Second, this is the end portion of a dendrite (see Vaughan and Peters, 1973). Again the dendrite is smooth, and only one of the synaptic junctions (1~) has a symmetric form. If this information is synthesized, the following statements can be made about these dendrites receiving degenerating geniculocortical afferents upon their shafts. The dendrites are relatively smooth in outline. The spines or protrubrances are only occasional and not nearly as common as those borne by pyramidal cell dendrites for example (see Vaughan and Peters, I973). Essentially, these dendrites have the features of those described previously in layer IV of the parietal cortex of the rat (Peters, 1971 ) . The most characteristic feature of these dendrites is the presence of frequent synaptic junctions along their shafts: the junctions are predominantly of the asymmetric variety. The range of size of these profiles is quite large, and unfortunately the cytoplasmic characteristics do not seem to be sufficiently constant so that they alone can always be useful in unequivocally identifying such dendrites in electron micrographs. Sometimes, as pointed out earlier (Peters, I97I), and as shown in Figs. I and 6, the microtubules may be more closely packed than in other dendritiC profiles, but in other cases (e.g. Fig. 4D) the converse is true. In fact a dendrite may be so swollen Fig. 8. A small neuron with a degenerating axon terminal (-~) synapsing with a thin dendrite (den). This dendrite is also shown in Fig. 9The nucleus (Nuc) of the neuron has an indented nuclear envelope and is surrounded by a thin rim of cytoplasm containing a few long cisternae of endoplasmic reticulum (ER) and small Golgi complexes (G). The perikaryon forms a few symmetric synapses with normal axon terminals (At). A degenerating terminal (d) lies immediately adjacent to the perikaryon. • I2OOO. 98 PETERS~ F E L D M A N and S A L D A N H A that the cytoplasmic contents are disrupted (Peters, i97i; Vaughan and Peters, 1973), although such swellings are less common in well-fixed than in poorly-fixed material. From the variety of sizes of dendrites which have been encountered with synaptic junctions formed on their shafts by degenerating terminals, it seems most likely that these dendrites can receive geniculocortical afferents anywhere along their lengths. However, of the axon terminals forming synaptic junctions along the five dendritic lengths shown here, only six are degenerating ones. The remaining 74 synaptic junctions are formed by normal axon terminals. Thus, in these reconstructions only about one in I2 of the synaptic junctions is formed by a degenerating geniculocortical axon terminal. Neuronal perikarya The available evidence indicates that the neurons in layer IV which possess smooth dendrites are the same ones that receive geniculocortical axon terminals on their perikarya. Thus, examples have been encountered in which smooth dendrites with the features described in the previous section, and a number bearing degenerating axon terminals on their shafts have been seen to emerge from perikarya (Figs. 8, 9, 13 and 14). Further, those same kinds of perikarya from which the smooth dendrites emerge have also been seen to form synapses with degenerating axon terminals (Figs. 1% n and 12). Such degenerating axosomatic synapses have asymmetric synaptic junctions. These neurons are of two types. The first type is a rather small neuron (Figs. 8, 9, I I and 12) that has a perikaryon about 15 ~m in diameter. The features of the perikaryon can be seen in both Fig. 8, which shows such a neuron with a dendrite bearing a degenerating axon terminal (Fig. 9) emerging from the perikaryon, and in Fig. I I in which a perikaryon receives a degenerating axon terminal (Fig. 12). The nuclei of this type of neuron (Figs. 8, IO and I1) have a relatively homogeneous karyoplasm which has a tendency to show a thin condensation of chromatin beneath the nuclear envelope. Frequently the rather ruffled nuclear envelope is indented (Figs. 8 and I I). The cytoplasm forms only a thin rim around most of the nucleus (Nuc), and seems to be rather darker than that of pyramidal cells. This is probably attributable to the comparatively large numbers of ribosomes that lie free in the cytoplasm. Other ribosomes are attached to the surfaces of cisternae of the granular endoplasmic reticulum (ER) which are often long and frequently lie singly, and parallel to the surface of the nucleus. Rather than forming a shell around the entire nucleus the Golgi apparatus (G) is usually present as isolated complexes which are preferentially located in those portions of the perikaryon where the cytoplasm is most abundant. The perikarya of these neurons (Figs. 8, IO and I I) form both symmetric and asymmetric Fig. 9. The dendrite of the neuron illustrated in Fig. 8. This thin dendrite (den) has closely packed microtubules (m) and is synapsing (-+) with a degenerating axon terminal (d). Two normal axon terminals (At) are also forming asymmetric junctions. • 38000. Fig. Io. Part of the perikaryon of a neuron showing part of its nucleus (Nuc) and the thin rim of cytoplasm containing many free ribosomes (r). One degenerating (d) and one normal (At) terminal are forming asymmetric synaptic junctions. • 50000. I00 PETERS, F E L D M A N and S A L D A N H A synaptic junctions with axon terminals. Both types of junctions are not always displayed in any one section through a perikaryon, and this is true of the perikaryon illustrated in Fig. 8. The axon terminals (At) seen to synapse with this perikaryon show only symmetric junctions, but a darkened axon terminal (d) that may have been synapsing with this perikaryon is close by. This point will be returned to again later. Although the magnification in Fig. I I is rather low, the perikaryon does have both symmetric and asymmetric synaptic junctions. Not all of the axon terminals forming asymmetric synaptic junctions with a perikaryon degenerate after geniculocortical lesions, as illustrated in Fig. IO, which shows a portion of the perikaryal surface of a neuron of this type. One of the axon terminals is degenerating (d) and an adjacent one (At), which is also forming an asymmetric synaptic junction, appears to be unaltered. As will be observed in Figs. 8 and 9, the dendrites emerging from this type of neuron are rather thin. In this particular example the dendrite is smooth surfaced and has closely packed microtubules (m) in its cytoplasm. It has very similar features to some of the dendrites reconstructed from the serial thin sections and is characterized by receiving axon terminals on its shaft. In addition to the degenerating axon terminal (d) there are two normal axon terminals (At) forming synaptic junctions with the dendrite. For the neuron shown in Fig. I I, only the base of a dendrite (den) is visible. As in the aforementioned example, this dendrite also emerges rather abruptly from the perikaryon. It does not possess a wide tapering base and from what can be seen of its morphology, this dendrite also appears to have rather closely packed microtubules in its cytoplasm. The second type of neuron has rather different features, and an example of such a neuron is shown in Fig. 13. This type of neuron has a slightly larger cell body than the first type and although it is difficult to be certain from electron micrographs it appears to be more oval. At least in the example shown here, the elongation is in a direction parallel to the vertical axis of the cortex. The nucleus (Nuc) is rather more scalloped in outline than that of the first type of neuron and in examples we have seen there is usually a prominent nucleolus present. T h e perikaryal cytoplasm forms a somewhat thicker layer around the nucleus and the Golgi apparatus (G) more completely encircles the nucleus. Cytoplasm is most abundant at the poles of the cell body from which rather thick dendrites (den) emerge. For the neuron shown in Fig. I3, the emerging dendrite is some 3 ~m thick and has a long tapering base. This is in contrast to the much thinner dendrite, which is only about I ~m thick, extending from the first type of neuron illustrated in Fig. 8. This thicker dendrite emerging from the second type of neuron has smooth contours, but the microtubules follow a wavy course, so that in transverse sections it can be assumed that the appearance would be somewhat like that of the dendrite shown in Fig. 2. Many axon terminals ( ~ s) synapse with the shafts of Fig. II. The cell body of a small neuron with an indented nucleus (Nuc) and a thin rim of perikaryal cytoplasm containing long cisternae of endoplasmic reticulum (ER) and a few Golgi complexes. (G). The cytoplasm of this cell body has many free ribosomes. Emerging from the bottom right is a dendrite (den). This perikaryon is receiving a degenerating axon terminal (d) that is further shown in Fig. z2. • z z o o o . Fig. I2. The degenerating axon terminal (d) is synapsing with the cell body shown in Fig. I I. This axosomatic junction is asymmetric. Note the vacuoles in the adjacent perikaryal cytoplasm. • 5oooo. IO2 PETERS, FELDMAN and SALDANHA these dendrites. At the base o f the dendrite these axon terminals are rather sparse and while the larger ones tend to form symmetric synaptic junctions, the small ones form asymmetric junctions. Towards the site where the degenerating axon terminal is located (Fig. 13, d and Fig. 14), axon terminals become more closely packed. As with the first type of neuron, the perikarya of this second type also forms both symmetric and asymmetric junctions. As mentioned earlier, in our preparations many profiles of the cell bodies of both types of neuron often have two or three degenerating axon terminals in their immediate vicinity (Figs. 8 and 13, -,s). However, only a few of these form definitive synaptic junctions with the perikarya. T h e others either form questionable synaptic junctions or merely lie adjacent to the perikarya. Nevertheless the association of degenerating axon terminals is so characteristic that we are prompted to suggest that such terminals once synapsed with the perikarya, but became detached during the postoperative interval. Discussion So far as we are able to determine, all of the synapses in layer IV which degenerating geni9 ~ . culocomcal terminals make with dendritic shafts and perikarya are accounted for by the two types of neuron described here. Both types have relatively smooth dendrites and their perikarya are characterized b y possessing both symmetric and asymmetric synaptic junctions. Both forms of synaptic junction also occur on the dendritic shafts o f these two neuronal types. Further, o f the asymmetric junctions, not all of those on the perikarya involve axon terminals that are caused to degenerate as a consequence of a lesion in the lateral geniculate nucleus. T h e same is true o f these on the dendrites, for only about one in I2 o f the latter are formed by affected axon terminals. T h u s , it seems that although these two types of smooth surfaced neurons in the rat visual cortex have geniculocortical axon terminals scattered over their dendritic trees and perikarya, they receive far less than their total afferent input from geniculocortical axons. At present the origins of these other axon terminals are completely unknown. A word of explanation about the terminology used here is necessary. As a n u m b e r of recent authors, including Szentfigothai (1973) and Jones (1975) have pointed out, in the present state of our knowledge, neurons in the cerebral cortex can essentially be classified as being o f two kinds: pyramidal neurons and others. T h e s e 'other' neurons can have a variety o f shapes, but as Jones (1975) emphasizes, on the whole they lack one or more criteria for pyramidal neurons. T h e most obvious criterion that they lack is an apical Fig. 13. The second type of neuron with smooth dendrites. The nucleus (Nuc) is rather scalloped in outline and has a prominent nucleolus. The perikaryal cytoplasm is quite thick and contains a Golgi apparatus (G) that is particularly prominent at the poles of the oval cell body. A thick dendrite (den) emerges from the upper pole of the cell and synapses with a degenerating axon terminal (d) shown at a higher magnification in Fig. 14. The positions of some of the normal axon terminals synapsing with this neuron are indicated with arrowheads9 Note the degenerating axon terminals (-+ s) lying adjacent to the perikaryon. • 54oo. Fig. I4. The degenerating axon terminal (d) synapsing with the dendrite (den) of the neuron illustrated in Fig9 13. x 600009 lO4 PETERS, FELDMAN and SALDANHA dendrite that ascends to layer I and branches into a distinct apical tuff. Various authors have referred to the 'other' neurons which lack this dominant apical dendrite as either nonpyramidal neurons, or stellate cells. We will use the term stellate cell here, since although the other term, non-pyramidal neuron, is more accurate it is cumbersome and no more informative. It should be borne in mind though, that only a few of these other neurons are star shaped, and that they may have spines extending from their dendrites (e.g. see Garey, z971 ; Lurid, I973, Szentfigothai, I973; Jones, z975). In fact many stellate cells have spiney dendrites. However, in the case of the neurons described here the spines are very few, and it seems reasonable to refer to the dendrites as being smooth, and hence to the neurons as smooth stellate cells. Smooth steUate cells with similar features to the ones described here have also been shown to be the recipients of thalamocortical afferents in a number of specific regions of the cerebral cortices from various animals. Thus, Strick and Sterling (1974) show that such neurons in the cat motor cortex receive axon terminals from the ventrobasal nucleus of the thalamus. However, although they find degenerating axon terminals to form asymmetric synapses with smooth dendrites which are characterized by the presence of other asymmetric and symmetric synaptic junctions on their shafts and by their content of closely packed microtubules, Strick and Sterling were not able to trace these dendrites to their cell bodies of origin. These authors nevertheless concluded that such dendrites take origin from perikarya which also receive degenerating axon terminals. Eight per cent of all degenerating axon terminals were located on the dendrites and perikarya of these stellate cells, and Strick and Sterling (I974) inferred that only the proximal portions of the dendritic shafts receive thalamocortical afferents. In the motor cortex of the monkey an electron microscopic study led Sloper (I973 a) to differentiate between two forms of stellate cell, a small one which is prevalent in layer II and a larger one that occurs in layers IV and V. In a subsequent study Sloper (I973b) made lesions in the thalamus and concluded that only the larger of these two stellate cells receives thalamocortical afferents, and that such neurons receive degenerating axon terminals both on their perikarya and dendritic shafts. As in our present study, Strick and Sterling (I974) find that some of the degenerating axon terminals synapsing with the stellate cells also form synapses with dendritic spines. Such a sharing of a degenerating thalamocortical axon terminal by these two forms of postsynaptic component was not encountered by Jones and Powell (I97o) in their study of the projections of the ventral nucleus of the thalamus to the cat somatosensory cortex. In addition Jones and Powell (I97O) find that as many as 25% of the degenerating thalamocortical axon terminals synapse with the shafts of smooth dendrites. Again, these smooth dendrites have other, and normal, axon terminals synapsing with their shafts. Jones and Powell (I97o) pass no comment upon the form of the perikarya giving rise to these smooth dendrites, although in a recent study of Golgi impregnated material Jones (I975) suggests that a kind of non-pyramidal neuron which he designates as a Type 5 cell is the one involved. Jones reports that such neurons are present in large numbers in layer IV and that only a few occur in other layers. These Type 5 neurons are the smallest ones present in the somatosensory cortex and seem to be identical with the neurons that Valverde (I97 I) refers Geniculo-cortical projection in rats. II Io5 to as 'clewed ceils' in the striate cortex of the monkey. The somata of the Type 5 cells are only about IO ~m in diameter and from them emerge thin dendrites which lack spines. In area 17 of the cat visual cortex Garey and Powell (I97 r) estimate that I4~ of the population of degenerating geniculocortical afferents form asymmetric synapses with dendritic shafts. Although the criteria used are not clear, these authors arrive at the conclusion that about half of these dendrites arise from stellate cells. Another 3% of degenerating axon terminals synapse with neuronal somata that sometimes receive more than one degenerating axon terminal in addition to several normal axon terminals which form both symmetric and asymmetric synapses. These authors obtain basically similar results in studies of the geniculocortical afferents to areas I8 and I9 of the cat and to area 17 of the monkey. Garey and Powell (I97 I) state that in addition to some of the dendrites that receive degenerating terminals on their shafts, the somata receiving degenerating terminals also belong to stellate cells. Colonnier and Rossignol (r969) also describe smooth stellate cells in area 17 of the cat that receive geniculocortical afferents on their dendrites and perikarya. From these studies it may be concluded that in various parts of the cortex and in different animal species, one common recipient of the specific thalamocortical projection is a smooth stellate cell which is present in layer IV. Neurons with such features have, as stated above, been encountered in Golgi studies of some areas of the cerebral cortex. For example, in the visual cortex of the monkey Valverde (I97 I) describes the clewed cells which are abundant in layer IV and which he considers to be postsynaptic to geniculocortical afferents. These small neurons have smooth and rather beaded dendrites. The axons of such neurons produce numerous collaterals that encompass a spherical domain. Similar neurons, Type 5 cells, have been described by Jones (I975) in the monkey somatosensory cortex, but Lund (I973) seems not to have encountered this type of neuron in her study of the monkey visual cortex. Unfortunately, so far as the rat is concerned, there are no systematic Golgi studies of the neurons in the cerebral cortex which would allow similar neurons to be identified with certainty. However, in an earlier study (Peters, I97 I) it was shown that there are two basic types of smooth stellate cells in layer IV of the rat parietal cortex. One of these neuronal types has a round cell body and thin, smooth dendrites that pass in all directions. The other has a more oval perikaryon and its dendrites, which tend to pass in a vertical direction, extend from the narrow ends of the cell body. These may be the two types of neurons encountered in the present electron microscope study, but additional work is necessary to establish this point. it should also be borne in mind that some of the smooth dendrites receiving geniculocortical afferents in layer IV may have their perikarya located in other layers. As an example of this situation reference may be made to the drawings in the article by Valverde and RuizMarcos (I969). These authors show a stellate cell with smooth dendrites whose perikaryon is located in layer III in the mouse visual cortex, but which they interpret as receiving geniculocortical afferents on its dendrites. Valverde and Ruiz-Marcos (I969) suggest that the axons of such neurons produce dense networks which are pierced by the pyramidal cell apical dendrites, upon whose spines the axons terminate. Since the synaptic junctions on such dendritic spines are asymmetric, it might be supposed, if the results obtained for the cerebellum (e.g. Uchizono, I965) can be extended to I06 PETERS, FELDMAN and SALDANHA the cerebral cortex, t h a t these synapses are excitatory. I n direct contrast, Jones (I975) suggests t h a t the d e n s e axonal n e t w o r k o f s u c h n e u r o n s is s u i t a b l e for exerting a p o w e r f u l i n h i b i t i o n . T h i s w o u l d seem to be s u p p o r t e d b y the work o f L e Vay (1973) who s t u d i e d G o l g i i m p r e g n a t e d n e u r o n s i n the visual cortex o f t h e cat a n d m o n k e y . L e V a y (1973) finds t h a t the axons o f the s p i n e - f r e e stellate cells f o r m s y m m e t r i c , or T y p e 2 s y n a p t i c j u n c t i o n s . Acknowledgements T h i s work was s u p p o r t e d b y g r a n t N S - o 7 o I 6 f r o m the N a t i o n a l I n s t i t u t e o f N e u r o l o g i c a l a n d C o m m u n i c a t i v e D i s o r d e r s a n d Stroke, o f t h e U n i t e d States P u b l i c H e a l t h Service. References BENE VEN T O, L. A. (1972) Thalamic terminations in the visual cortex of the rhesus monkey and opossum. Anatomical Record I72, 268. CLARK, W. E. 5. (1932) An experimental study of the thalamic connections in the rat. Philosophical Transactions of the Royal Society of London, Series B 222, 1-28. COLONNIER, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Research 9, 269-87. COLONNIER, M. and ROSS IGNOL, S. (1969) Heterogeneity of the cerebral cortex. I n Basic Mechanisms of the Epilepsies (edited by JASPER, H. H., WARD, A. A. and POPE, A.), pp. 29-4o. Boston: Little, Brown. GAREY, L. J. (1971) A light and electron microscopic study of the visual cortex of the cat and monkey. Proceedings of the Royal Society of London, Series B 179 , 21-4o. GAREY, L. J. and POWELL, T. P. S. (1971) An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proceedings of the Royal Society of London, Series B I79, 41-63. GRAY, E. G. (1959) Axosomatic and axodendritic synapses of the cerebral cortex.Journal of Anatomy 93, 420-33. H ~JBEL, n. H. and w I Es EL, T. N. (I 962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.Journal of Physiology 16o, IO6-54. HUBEL, D. H. and WIESEL, T. N. (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146 , 42 I-5O. JONES, E. G. (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey.Journal of Comparative Neurology 16o, 205-68. JONES, E. G. and POWELL, X. P. S. (1970) An electron microscope study of the laminar pattern and mode of termination of afferent fibre pathways in the somatic sensory cortex of the cat. Philosophical Transactions of the Royal Society of London, Series B 257, 45-52. KRIEG, W. J. s. (I946) Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas. Journal of Comparative Neurology 84, 22 I-76. LASHLEY, K. S. (1934) The mechanism of vision. VIII. The projection of the retina upon the cerebral cortex of the rat. Journal of Comparative Neurology 60, 57-79. LASHLEY, K. S. (1941) Thalamo-cortical connections of the rat's brain. Journal of Comparative Neurology 75, 67-I2I. LE VAY, S. (I973) Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations. Journal of Comparative Neurology 15o, 53-86. L ~:ND, I. S. (1973) Organization of neurons in the visual cortex area 17 of the monkey (Macaca mulatta). Journal of Comparative Neurology I47, 455-96. PETERS, A. (I97 I) Stellate ceils of the rat parietal cortex.Journal of Comparative Neurology 141, 345-74. Geniculo-cortical projection in rats. II lO7 PETERS, A. and FELDMAN, M. L. (1976) T h e projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. I. General description.Journal of Neurocytology 5, 63-84. P o L L EY, E. H . ( 1971 ) Intracortical distribution of lateral geniculate axons in cat and monkey. Anatomical Record 169, 4o4. RIBAK, C. E. and PETERS, A. (1975) An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Research 92, 341-68. ROSENqUIST, A. C., EDWARDS, S. B. and PALMER, L. A. (1974) An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the cat. Brain Research 8o, 71-93. SLOPER, I. J. (I973a) An electron microscope study of the neurons of the primate motor and somatic sensory cortices.Journal of Neurocytology 2, 35 I-9. SLOPER, J. J. (I973b) An electron microscope study of the termination of afferent connections to the primate motor cortex. Journal of Neurocytology 2, 36 I-8. STRICK, V. L. and STERLING, P. (1974) Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscope study. Journal of Comparative Neurology I53, 77-IO6. SZENTAGO THAI, J. (1973) Synaptology in the visual cortex. In Handbook of Sensory Physiology, Volume VII~3 Central Processing of Visual Information. Part B. Visual Centers of Brain. (edited by JUNG, R.), pp. 269-324. Berlin: Springer-Verlag. UCI-IIZONO, K. (I965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature (London) 207, 642-3. v AL VERDE, F. ( 197 I) Short axon neuronal sub systems in the visual cortex of the monkey. International Journal of Neuroscience x, 181-97. VALVERDE, F. and RUIZ-MARCOS~ A. (1969) Dendritic spines in the visual cortex of the mouse: Introduction to a mathematical model. Experimental Brain Research 8, 269-83. VAUGHAN, D. W. and PETERS, A. (I973) A three-dimensional study of layer I of the rat parietal cortex. Journal of Comparative Neurology I49, 355--70WALLER, W. H. (1934) Topographical relations of cortical lesions to thalamic nuclei in the albino rat. Journal of Comparative Neurology 6o, 237-70. w E ST RUM, L. E. (1973) Early forms of terminal degeneration in the spinal trigeminal nucleus following rhizotomy.Journal of Neurocytology 2, I89-215.