Download The projection of the lateral geniculate nucleus to area 17 of the rat

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
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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.
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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
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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.
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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
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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
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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.
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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.
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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.
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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 ~
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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
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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.
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