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Regarding Several Points of Doubt of the Structure of the Olfactory BulbAs Described by T. Blanes

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THE ANATOMICAL RECORD 291:751–762 (2008)
Regarding Several Points of Doubt of
the Structure of the Olfactory Bulb:
As Described by T. Blanes
CATHERINE LEVINE* AND ALEXANDER MARCILLO
The Miami Project to Cure Paralysis, University of Miami Miller School of Medicine,
Miami, Florida
ABSTRACT
In order to complement the studies on the fila olfactoria completed by
Dr. Santiago Ramón y Cajal, we have included a translation of ‘‘Sobre
Algunos Puntos Dudosos de la Estructura del Bulbo Olfatorio’’ by
T. Blanes, a student of Dr. Cajal. This work describes in stunning detail
additional morphological aspects of the olfactory pathway, including what
was at the time the modestly studied neuroglia. The neuroglia of the olfactory system has been revisited in the last several decades for its importance in the field of regenerative neuroscience. Olfactory ensheathing glia
has the unique quality of providing ensheathment to neurons which traverse from the central to the peripheral nervous system and are being
used as a candidate in present-day transplantation studies to mimic this
phenomenon at the dorsal root entry zone after a central nervous system
injury. Although this fine work has passed its centennial anniversary
since initial publication, it has been widely cited throughout the years,
and of recent when Pressler and Stowbridge reported Blanes cell electrophysiological recordings (Neuron V 49, 6; p 889–904, 2006). An English
translation the details of what Blanes initially documented with unduplicated precision can now be made available to a wider audience in the
field of neuroscience, and is especially important now that more and more
present-day studies require a precise and complete understanding of the
anatomical structures contained within the olfactory system. Anat Rec,
291:751–762, 2008. Ó 2008 Wiley-Liss, Inc.
Key words: olfactory system; mitral cells; granules; neuroglia
The original title, ‘‘Sobre Algunos Puntos Dudosos de
la Estructura del Bulbo Olfatorio’’ by T. Blanes, Pupil of
Medicine at the Medical Faculty of Madrid was published in 1898 (Revista Trimestral Micrográfica 3:99–
127). Here, it has been translated and interpreted from
the 19th Century Spanish Original by Catherine Levine
and Alexander Marcillo, from The Miami Project to Cure
Paralysis, University of Miami Miller School of Medicine, Lois Pope LIFE Center, 1095 NW 14th Terrace,
Miami, Florida.
After the fundamental and important research of
Golgi (1) and Cajal (2), the fine anatomy of the olfactory
bulb seemed completed along general lines; the subsequent work carried out by Pedro Ramón (3), van
Gehuchten and Martı́n (4), Retzius (5), Calleja (6), and
Kölliker (7) has served most of all to establish the morphology of the diverse bulbar elements in animals, and
Ó 2008 WILEY-LISS, INC.
perfect, in some secondary aspects, our notion about the
structure and functionalism of the olfactory system in
man and superior mammals.
The figures were reproduced and modified for clarity with the
permission of, and are copyrighted to Herederos de Santiago
Ramón y Cajal.
*Correspondence to: Catherine Levine, The Miami Project to
Cure Paralysis, University of Miami Miller School of Medicine,
Lois Pope LIFE Center, 1095 NW 14th Terrace, 5th Floor,
Miami, FL 33136. Fax: 305-243-2691.
E-mail: clevine@med.miami.edu
Received 17 May 2007; Accepted 11 January 2008
DOI 10.1002/ar.20680
Published online 2 April 2008 in Wiley InterScience (www.
interscience.wiley.com).
752
C. LEVINE AND A. MARCILLO
When it comes to the physiology of the bulb, almost
all scholars, without reservation, accept the dynamic
schema thought up by Cajal, because he is the only one
whose findings are in agreement with the facts. For the
creation of this schematic, our Professor solely took into
account the examination of microscopic preparations; all
bias of teaching and all theoretic commitments were dismissed beforehand. Therefore, it is not strange that the
most valuable authorities of neurology, such as Retzius,
Lenhossék, van Gehuchten, His, Edinger, and even Kölliker himself, (who previously refuted the conductive
role of dendrites), enthusiastically accept conduction as
a mechanism for olfactory excitation, based on the new
facts contributed by Cajal, among these, the demonstration that the fibers received from the olfactory mucosa
do not pass the olfactory glomeruli, where they create a
relationship through contact with the tufts of the dendritic terminals of the mitral and tufted cells.
It is clear that Cajal did not have the illusion that his
would be the final word on the subject; he knows a great
deal, and through unfortunate experience, he knows
how far opposing resistance to new ideas can reach
because of excessive narcissism, and because of culture,
eminently egotistical toward the scientific consequence;
moreover, it is well known that the most sovereign talents are precisely the ones that are most hostile to all
innovation. Thus, he never had the pretentiousness to
try and convince those illustrious scholars, which, like
Golgi, are noted for passionately and prematurely
defending scientific hypotheses that were completely irreconcilable with the ideas of the histologist of Madrid.
Nor did he ever expect to attract to his team the Italian
neurologist’s enthusiastic disciples L. Sala and Monti,
both of whom had a perfectly justified affection and admiration toward their teacher, which one can presume
may have allowed them to forego the serenity of the
impartial judgment necessary to examine reformist
doctrines.
But objections themselves, wherever from, are always
respectable and should all be the focus of an attentive
exam. Therefore, we will try to examine in the present
work all of the open questions regarding the structure
and activity of the olfactory bulb, clearly and calmly
studying the facts alleged by the various authors, without being persuaded by any other purpose than the
enlightenment of the truth. To better achieve this commitment, we have dedicated 2 years to the study of
the structure of the olfactory bulb, having, therefore,
completed an infinite number of preparations, as much
as with Ehrlich’s method as with Golgi’s Method. To
compare them with ours, we have had at our disposal all
of Cajal’s and Calleja’s collection of preparations concerning the anatomy of the aforementioned organ, and
we believe that, at least for the explanation of some of
the problems waiting to be solved, our opinion will not
be lacking in value. The material of study has consisted
of rats, mice, and most of all cats, from the moment of
their birth to adulthood.
NATURE OF THE GRANULES OF THE
OLFACTORY BULB
It is known that between fascicles of anteroposterior
nerves, the region of the white matter of the bulb contains numerous islets made up of small triangular or
ovoid corpuscles, originating from central and peripheral
expansions, among which, as already recognized by
Golgi, it is not possible to find any that possess axonal
characteristics.
Cajal completed a detailed study of these cells, demonstrating their perfect radial orientation and revealing an
important fact: the peripheral expansion, almost always
the thickest, proceeds continuously to the molecular
layer and forms an elegant tuft in its thickest portion,
whose appendices, notably spiny, come in contact with
the dendrites of the medial and inferior mitral and
tufted cells. Because this expansion possesses a fixed
relationship, and the body and central appendices seem
to be in contact with centrifugal fibers, Cajal is inclined
to consider, from a functional nature, the aforementioned prolongation, according to the theory of dynamic
polarization, must function like an axon and not like a
dendrite. All of which naturally involves the idea of considering the granule as a species of nervous corpuscle,
in a whole comparable with amacrine or retinal spongioblast cells, elements that are undoubtedly nervous,
although void of a functional expansion, or rather, of differentiation into two categories of expansions.
Concerning this opinion of Cajal, and any of the facts
from which it is founded, several objections have been
raised, of which we will demonstrate their total lack of
foundation.
1. It has been said by van Gehuchten and Kölliker (7),
that the peripheral tuft of the granules extends, in
effect, in the vast majority the cases, as Cajal asserts, to
the molecular layer; but in a few corpuscles, are
observed to end on the mitral cells, that is, in the granule layer. We have carefully examined a large number of
embryonic and adult granule preparations, and have
become completely convinced of the reality of Cajal’s
findings; the peripheral expansion always sends its tuft
to the molecular layer. Certainly, in some granules, this
stem does not pass the level of the mitral cells, but the
careful observation with a 1.30 apochromatic objective,
proves in an impervious way that, in these corpuscles,
the stem has been impregnated in an incomplete mode:
the end of the aforementioned expansion ends up
brusquely without ramification; and the error of van
Gehuchten and Kölliker, has involved considering the
set of collateral branches, as a definite terminal arborization, emitted from the stem before its artificial interruption. In our own preparations, and even in Kölliker’s
drawings, we can suspect the cause of this error (see
Fig. 763 in this scholar’s text), although it may have
also happened that the aforementioned author may have
identified a dislocated epithelial corpuscle as a granule
cell. This brings us to a point to add some details
regarding the morphology of the granules, details that
must be kept in mind to avoid all mistakes between the
granules and the epithelial cells.
Body
The body of the granule presents in one of two modes:
smooth and bristly with small spines or short and irregular outgrowths. The smooth soma, appears in the thickness of the islets (Fig. 1A), in contact with other granules, and it is not rare to see it faceted with reciprocal
pressure. The smoothness of the body of these central
granules, and the scarce quantity of protoplasm that
REGARDING SEVERAL POINTS OF DOUBT OF THE STRUCTURE OF THE OLFACTORY BULB
753
tory, until it reaches the mitral cells, presents quite a
spiny contour during its passage through the nervous
plexuses, and a smooth surface as it crosses the islets.
As it passes the mitral cells, it either loses its spines, or
it notably reduces them, recovering them and extraordinarily exaggerating them at the level of the terminal
tuft. The collateral branches, that at a sharp angle supply some stems for the granular zone, do not end in the
islets, but in the nervous bundle, and also display a
spiny contour.
Central Expansions
Fig. 1. Granules of the olfactory bulb of the 20-day-old cat. Golgi’s
Method. A: Smooth body of a granule resting in the center of a cell
grouping. B: Peripheral granule with spines. C,D: Spiny granules. E:
Voluminous granule. F: Peripheral granule of the mitral cell layer. G:
Tiny granule located in the mitral cell layer. H: Dislocated mitral cell.
surrounds the nucleus, is an indication that pericellular
arborizations do not exist in the thickness of the islets.
Aside from this, Cajal in his extensive work on the Nervous Centers (8), underscores this particularity, and cites
the bipolar cells of the retina, in acknowledgment that
somas poor in protoplasm do not tend to possess nervous
nests (shells). On the other hand, all bordering granules
or those lateral of the islets, like those separately
grouped in the nervous plexuses, exhibit numerous
points of roughness. In the immediate bordering cells,
the surface that faces the interior of the islet is also
smooth, and rough at the border of the nervous plexuses
of the white matter (Fig. 1B). A worthy fact to also note,
which confirms Cajal’s aforementioned hypothesis on the
importance of conduction of the perisomatic protoplasm,
it is that the marginal granules and the isolated granules possess more protoplasm than the central ones
belonging to the islets. There is, however, an exception.
Let us finish this brief description of the soma, adding
that its size can be quite variable, and in light of these
large differences in diameter, it would be pertinent to
separate the granules into small, medium, and large.
Peripheral Expansion
As it has already been well described by Cajal,
Retzius, van Gehuchten, and Kölliker, we will add
merely a minutia to the facts set forth by these scholars:
The aforementioned expansion, in its complete trajec-
In number, these appear as one, two, three, and rarely
four. These expansions are also spiny, as van Gehuchten
indicates, and they diverge in a fan-shape, splitting and
getting lost in the thickness of the nervous plexuses.
According to our observations, these branches never end
at the islets, noting that, as the branches cross the
islets, they present a smooth contour equal to the peripheral expansion. There is a relation between the position of the granule and the length of these expansions:
the granules situated close to the mitral cells, exhibit
long and richly branched central expansions, while those
that are more profound, bordering the zone of the epithelial corpuscles, exhibit shorter and more rudimentary
central expansions. However, these expansions are never
as short, branched, and numerous as those characteristic of the epithelium or the neurological elements.
Because of not attentively considering these differences,
Kölliker incorrectly identified both categories of elements, that is, the epithelial cell and the granule.
All of our efforts to find a central expansion that can
morphologically be considered as an axon have failed;
regarding this point, therefore, we find ourselves completely in agreement with Golgi, Cajal, Retzius, van
Gehuchten, and P. Ramon. Therefore, it is no surprise
that in a recent work by Hill (9), he believes to have
come across the axon of the granules. The simple inspection of the figures annexed to this author’s text plainly
reveal that the elements that have intruded on the
axon, are not legitimate granules, but short axis–cylinder cells (also called inferior tufted cells), previously
described by Golgi, Cajal, and van Gehuchten. In this
way, of the two types of granules with an axon, the one
that Hill cites as type 1 (Fig. 2 of his work), undoubtedly
Fig. 2. Small periglomerular nerve cells of the 1-month-old cat (superficial granules of Kölliker). a: Bifurcating axon. b: Cell whose axon
emits collaterals descending toward the interglomerular spaces. c:
Description for cell c was omitted in the original. d: Cell whose fine
axon appears to end at a short distance in two branches. e: A cell
with three descending branches.
754
C. LEVINE AND A. MARCILLO
Fig. 3. Biglomerular nerve cells of a 1-month-old cat. A: Cell that
seems to branch out into three glomeruli. B,D: Biglomerular cells. C,E:
Monoglomerular cells. a. Axon.
correspond to short axon cells described by Cajal (see
upcoming description), and those reproduced in Figure 3,
under the name type 2 granules, represent stained dislocated mitral cells described by van Gehuchten.
2. Is the granule a neurological element? In light of
the morphologic resemblance of the granule with the
epithelial cell, of the transitions between both classes of
elements, of the absence of the functional expansion,
and so on, Kölliker considers, taking into account Cajal’s
opinion, the olfactory bulb’s granules as legitimate neuroglial cells. With reference to histogenesis, this scholar
affirms that the deepest granules may originate from
the epithelium and represent epithelial dislocated and
somewhat modified cells, while the most superficial
granules would be the progeny of ectodermal cells, destined to transform directly into spider like elements or
Deiters’s cells.
On the origin of the granules, our studies are not sufficiently complete to release a sound opinion; regarding
the identification of the granule with the epithelial or
neuroglial corpuscle, we will illustrate several reasons
that we expect will contribute to clarification of the
question at hand:
1.a It is known than Ehrlich’s method (methylene blue
by injection, Dogiel’s or Bethe’s fixation, and so on), does
not color neuroglia, only cells and nerve fibers. We find
authentic testimony of this truth in the memoirs of Arnstein, Smirnow, and, above all, of Dogiel. Nor has Cajal
been able to stain the aforementioned elements with
methylene blue (pure Ehrlich’s method); only with a special staining method (method of anaerobic action of
methylene blue) were the epithelials of the retina and
encephalons of certain vertebrates impregnated. On the
other hand, mammalian Deiters’ cells always gave the
appearance of being refractory, regardless of the method
of methylene blue staining used.
However, the aforementioned Ehrlich’s method, consistently and with great ease stains granules in the dog,
rabbit, and cat, animals that we have made numerous
tests in. The soma, acquires an intense blue shade, as do
the expansions, a singularly descending expansion can
continue on to the molecular zone, where it arrives at its
terminal tuft. Only in this tuft, as Cajal has demonstrated in other cells stained with methylene blue, the
spines cease to appear clearly, disappearing, without a
doubt, because of the intense varicose alteration provoked by air or other conditions that remain enigmatic.
The protoplasm of these granules behave, in the presence
of the methylene blue, like that of nerve cells, and
although they are stained much easier than the tufted
cells, according to this point of view, they are comparable to retinal spongioblasts, singular, avid elements of
methylene blue.
2.a There is a complete discrepancy between the neuroglial and epithelial granule. In Figure 8 (current
work), the epithelial cells and neuroglia of the olfactory
bulb are shown, and in Figure 1, the principal types of
granules are revealed. Compare both figures and it will
be evident that granules cannot be considered as neuroglial or epithelial elements. Noting the differences of general form, orientation, and connections, there are several
details that defy all confusion: (a) The soma of the granule always possesses ascending expansions, long and
divided into branches; the epithelial cell does not tend to
possess these; (b) The granule is smooth, or at the most
it exhibits some short spines, rarely divided into
branches; meanwhile, the soma of the epithelial and neuroglial cell appear bristly with a vast amount of varicose
appendices, very fine, divided into branches, distributed
throughout in partitions or small interstitial sheets, the
whole of which forms about the soma, an extremely thick
atmosphere of granules (Fig. 8c); (c) The granule’s peripheral stem only possesses certain short, unbranched
spines, like the protoplasmic stems of the nerve cells;
while the stem of the epithelial cell that shares the same
name exhibits, at the level of the white matter plexuses,
many laminar prolongations similar to winding shrouds
divided into branches, which form about the nerve fibers
a system of alveoli, comparable in all its parts to those
formed by the epithelial corpuscles of the retina and
Bergman fibers of the molecular layer of the cerebellum;
(d) finally, the granule has a tiny soma, poor in protoplasm, so much so that it is translucent allowing the
light brown stained nucleus to show through the cell,
unless the epithelial or neuroglial cell possesses a voluminous cell body copious in protoplasm, through which
the nucleus would always be imperceptible.
Many other reasons challenge the opinion of Kölliker:
The perfect orientation of the granules, the continuity of
its relationship with the dendritic plexus of the molecular layer, and, most of all, the large number of these corpuscles existent in the olfactory bulb of all vertebrates.
In fact, the granules are not missing, as Pedro Ramón
has demonstrated, neither in fishes, reptiles, and batrachians, where it is doubtful that genuine neuroglial corpuscles exist at any level; and indeed in these animals,
instead of looking like epithelial elements (the only representation of neuroglia in the inferior vertebrates), they
differ from these more so than in mammals, because
they lack any type of central appendix and have a perfectly smooth body. Calleja has also seen their smooth
appearance possessing only peripheral expansions in the
urodelan (Pleurodeles waltl).
All of the expressed facts are of great importance for
the appreciation of the physiological role of the granule,
and our teacher’s foresight is credited with considering
this element as a homolog of retinal spongioblasts.
Because granules are lacking a central expansion in
fishes, batrachians, reptiles, and birds, there is no other
remedy than to consider them as amacrine cells, of
REGARDING SEVERAL POINTS OF DOUBT OF THE STRUCTURE OF THE OLFACTORY BULB
centrifugal conduction, unless the doctrine of dynamic
polarization is disregarded; if it is reasoned that they
conduct from the terminal tuft to the soma, it would be
necessary to admit that impulses emerge from the soma
and pass to neighboring nerve fibers, an idea that struggles against everything that modern studies teach us
concerning the dynamism of the nerve cells. The mammalian granule represents an amacrine corpuscle,
which, because of reaching a more elevated phase of
perfection and differentiation, has augmented its collecting apparatus, adding to the soma and principal stem
a collection of dendrites or expansions of centripetal
conduction.
If the granule possessed a genuine axon, the problem
of its physiology would have an easy solution. It would
simply involve admitting that the central expansions as
well as the peripheral expansions have receptor-like
character and that the recollected impulses come from
the infinite collaterals that the axons of the mitral cells
and tufted cells scatter about the molecular layer and
nervous plexuses of the granules. But the absence of an
axon compels us to explore other explanations.
One of these explanations, which is quite rational and
has been mentioned in various writings by Cajal, assigns
these cells to the category of retinal spongioblasts, and
assumes that granules orient themselves, in the same
way as these corpuscles do, in the same relation to the
soma as the expansions, with centrifugal fibers from
which a current is propagated to the dendrites of the mitral and tufted cells. In this way, a motor impulse could
be projected onto the glomeruli, an action represented
by an intimate relationship between the terminal tufts
and the arborization of the olfactory fibers, perhaps
increase the strength of the discharge of the tufted cell
dendrites, with a resulting discharge brought about,
having a more energetic and diffuse reception of the olfactory impulse.
These are all conjectures that cannot be proven or disproven, because unfortunately the physiological methods
are too unrefined to allow us to attempt experimental
verification. Sustained in mere analogies, its value would
increase tremendously if the action of the brain on the
nerve endings and dendrites of the first junctions of the
sensory nerves, recently defined by Duval (10) and
Manouelian (11) under the name of the nervi-nervorum
theory, could be demonstrated in other nervous systems.
Kölliker’s Superficial Granules
According to Kölliker, tiny corpuscles rest around the
olfactory glomeruli. These corpuscles are pear-shaped,
triangular, or stellate, and have branches that penetrate
into the glomeruli, contributing even further to the intricacy of their existing plexus. Additionally, the lack of an
axon in one area, and the compactness of the soma in
another area, has served to incline the aforementioned
scholar to consider these cells as true granules, and consequently as a variety of neuroglial corpuscles. Furthermore, these cells were also seen by Cajal, who regarded
them as nervous system cells and even believed to have
distinguished a functional expansion in them, which
would target nearby glomeruli (2).
We have been able to perfectly stain these cells in
many preparations of the cat, dog, and rabbit. Additionally, our teacher Cajal has recently provided us with a
755
series of slices of the bulb of the 1-month-old cat, in
which these aforementioned tiny corpuscles appear by
the hundred, these were perfectly stained, with the
exclusion of the tufted cells. From the study of these
preparations, we have concluded that the superficial
granules cited by Kölliker are true nervous elements,
belonging to Golgi’s sensory type, designated by Cajal as
short axon neurons.
These cells are quite small, they do not exceed 6 to 8
microns in diameter; their shape is ovoid, spherical, or
polyhedral; they preferentially rest in the contour of the
glomeruli in the interglomerular spaces. They are also
dispersed above and below the glomeruli, very close to
the most peripheral tufts. Few reside in the glomerulus
itself, as Cajal already observed, these being preferentially in the cortical layers.
From the point of view of its dendrite distribution, two
types of periglomerular cells can be distinguished: the
monoglomerular type and the bi- and polyglomerular
type. The monoglomerular type is the most common. Its
dominant form is stellate, but it is not uncommon to find
it somewhat pear-shaped, semilunar, and even fusiform.
The elements that are fully stellate with multiple stems
tend to reside in the thickest area of the glomerulus,
preferentially in the cortical regions, while the pyriform
variety lies externally in the interglomerular spaces.
The scarcity of protoplasm is so much so that the nucleus can be perfectly distinguished. The dendrites,
which alternate between five or six in number, penetrate
and spread throughout the glomerulus, they branch out
prolifically, and generate a dense plexus of fine, nonspiny varicose bunches. Some, however, present expansions, like villi, that is to say, are covered with relatively
long appendices, sprouted at an acute angle.
Each glomerulus can possess branches containing
four, five, or more of these elements (Fig. 3C). There are
cells whose branches are moderate in secondary and
tertiary branching, only occupying a limited area of
the glomerulus; other elements possess more intricate
ramifications.
The biglomerular type tends to reside between the glomeruli. They generally consist of stellate or fusiform
cells, which can sprout into two stems, each of which
can branch out into a nearby glomerulus (Fig. 3D), or
three stems, of which two can distribute themselves in
one glomerulus and the third in another (Fig. 3B). The
mode of ramification is analogous to the aforementioned
monoglomerular cells; all of its branches are destined to
the thickest area of the glomerulus, which is an important detail that allows the separation, at first glance, of
certain elements of the inferior tufted cells which were
well described by Cajal.
The axon is very difficult to stain and even more difficult to track, not only because of its thin structure, but
also because of its irregular and contoured trajectory.
The rarity of the axon being stained and the difficulty of
recognizing it, in many cases among the mare magnum
(Great Ocean) of the fine dendrites sprouting from the
soma, have been without a doubt the reasons for which
Kölliker has not managed to distinguish it. We must,
however, confess that, even in the best preparations, a
good number of these corpuscles do not show even the
slightest sign of an axis–cylinder; but because this
expansion appears clearly in cells that are exactly the
same in size, position, and behavior as those that do not
756
C. LEVINE AND A. MARCILLO
Fig. 4. Peripheral tufted cells and periglomerular cells. A,B: Axons
of peripheral tufted cells with peripheral collaterals. C: Axon of a periglomerular cell. D: An axon that delivered initial branches toward the
periphery of the glomerulus of origin. E: Cell whose axon appears to
end up inside a distant glomeruli.
exhibit it, is impossible to dismiss the idea that the lack
of an axon is simply a defect of staining.
Figures 2–4, reveal the details of the pathway and
branching of the axon of the superficial granules. In general, the axon sprouts from the peripheral or smooth end
of the soma, makes one or two initial turns and then
becomes more or less horizontal, contouring through the
glomeruli, and frequently underneath these, at times
reaching very long distances. In these axons, we have
never come across the tendency to penetrate into the molecular layer, which is an important finding that separates them from the sprouts of the tufted cells, which as
we know, possess a pathway that is resolutely central.
At its horizontal trajectory through the granules, the
fine axons of the periglomerular elements supply an
intricate course of delicate collaterals (Figs. 2, 4), the
majority of which connect with the glomeruli, spreading
and branching out in its interstices. We have thought
that, in some cases, these collaterals made their way
into the glomeruli and arborized in them (Fig. 4D). We
would not, however, affirm this resolutely, as it is difficult to determine, in Golgi’s preparations, when the glomeruli appear without staining, if a fiber passes on top
or through them.
The collaterals as well as the terminal branch make
multiple turns, and after doing so end up at a varicosity,
an arborization deprived of large branches, well situated
in the glomerular interstices, either under or on top of
these. Some axons bifurcate near their origin, as occurs
in Figure 2a, and theses branches follow a path in the
opposite direction of each other, supplying collaterals for
groups of distant glomeruli. Other times, the division of
the axon generates a branch situated inside and another
outside of the glomerulus, both of equal direction and
endowed with collaterals.
Regarding the axon and its multitude of collaterals, it
would be pertinent to distinguish two types of cells: the
moderately robust, whose very long and horizontal axon
supplies collaterals that branch into a row of glomeruli
(Fig. 2b,e); and the smaller sort, which have delicate
axons that are difficult to stain, which abandon themselves in the immediate interglomerular interstices,
after having emitted only two or three collaterals.
What dendrites do the nervous arborizations of the
aforementioned cells connect with? For us, it is without
a doubt that the majority of the mentioned nervous
branches find themselves destined toward the body and
dendrites of the inferior tufted cells, which, although in
small number, inhabit the area between the glomeruli,
and even between these and the olfactory fiber layer. In
this way, the excitation gathered by the peri- or intraglomerular cells in the glomerular layer, would be able to
spread out transversely reaching long distances, involving in the conduction many tufted elements that are
very far apart from each other. In summary, the superficial granules of Kölliker, correspond to what Cajal has
called association cells (cerebellum and brain) and what
may be better termed dispersion cells or dissemination
of impulse cells.
Glomerular interstices possess other nerve fibers as
well. In Figure 4, we have reproduced some of these,
emanating from the axons of the most peripheral tufted
cells. These collaterals, which can be designated as the
peripheral collaterals of the tufted cells, sometimes rise
from the border of the molecular layer to the interglomerular spaces, and pass transversely thorough these
during long trajectories, giving off few small branches,
resembling arborization, in the aforementioned interstices. At times, the axon of the tufted cells initially
runs horizontally, passing two or three glomeruli, and
before turning into the molecular layer, generates a peripheral or interglomerular collateral (Fig. 4A,B).
To summarize, the inter- or intraglomerular spaces
contain a plexus of nerve fibers, the majority being nonmyelinated, composed of three factors: (1) peripheral collaterals of the most superficial tufted cells; (2) collaterals
and terminals of the granules, or small periglomerular
corpuscles, both small and large; and (3) a horizontal
trajectory, which is at times something recurrent when
stemming from the initial portion of the axon of the
tufted cells. Because these horizontal trajectories are
observed mostly under the glomeruli, between the glomeruli and the molecular layer, and because we also
find the long axons of certain periglomerular corpuscles
in this area, a nervous plexus is constructed here, which
is rich, and partially medullated, as we see in the Weigert-Pal preparations, whose dominant fibers advance
parallel to the cortex, in all directions, but always in the
same plane.
NERVE CELLS OF THE GRANULAR LAYER
According to the evident research of Golgi and Cajal,
the nervous plexus of the granular layer accommodates
various nervous corpuscles, of which, we will be able to
distinguish by the behavior of the axon in several varieties of cells: (1) Golgi cells, that is, corpuscles whose
axon arborizes in the nervous plexuses of the white matter; (2) Cajal cells, namely, those whose axons reach the
periphery, branching out into the molecular layer; and
(3) dislocated mitral cells or cells of van Gehuchten.
All of these cell types appear in our preparations. We
will not circumstantially report on these cells to avoid
repetition of explanations that have been masterfully
presented by the aforementioned scholars. At this time,
we will simply present a succinct review.
REGARDING SEVERAL POINTS OF DOUBT OF THE STRUCTURE OF THE OLFACTORY BULB
Fig. 5. Cells of the olfactory bulb of the 20-day-old cat. a–c: Dislocated mitral cells. d: Short axon cells with numerous dendritic expansions. e: Conventional mitral cell whose axon emanates from a dendrite. f: Small mitral cell that supplies a delicate tuft into the glomerulus. g,h: Small tuft emanating from a dislocated mitral cell.
Dislocated Mitral Cells
These cells were very concisely mentioned by van
Gehuchten without detail; these cells deserve to be
described in detail, because in our opinion, its morphology can shed light on the functional value of the spiny
appendices found on dendrites, at the same time they
confirm the law of saving space established by Cajal,
which offers us noteworthy information about the retina
and the cerebellum.
The first thing that calls one’s attention about these
cells (which lie in various planes of the internal molecular layer, and even in the nearby white matter plexuses),
is that they are not found in all mammals, or at least
their distribution varies appreciably among diverse species. We have yet to find them in the rabbit, rat, or
mouse. In Cajal’s collection on these animals, not even a
corpuscle of this sort is seen. On the other hand, they
are quite abundant in the cat, to the point of almost
touching laterally in certain areas of the olfactory bulb
(Fig. 5b,c). They must be quite scarce in the dog, as, in
many preparations, only two have been stained, and
even these rest not far from the row of legitimate mitral
cells. The dislocated mitral cells faithfully conserve the
disposition and connections of the dendrites of the con-
757
ventional mitral cells. One of the expansions of these
cells, generally the most robust, directs itself to the periphery, crosses the mitral cell and molecular layers, and
ends at an intraglomerular tuft. In its journey through
the superficial molecular layer, it can extend collateral
branches, which are connected with the tufts of the deep
granules, throughout this zone.
(1) The internal or lateral dendritic expansions often
follow an arch of variable radius reaching the mentioned
molecular layer and distributing themselves in the same
way as the conventional mitral horizontal dendrites.
(Those who do not believe in the conductive property of
dendrites must ponder upon this fact that confirms,
even in the dislocated cells, that the connections do not
change.) No protoplasmic branch seems to be destined to
gather impulses at the deep molecular layer or in the
nervous compartments, which proves to be particularly
interesting. Additionally, no dendrite possesses spiny collateral appendices.
This last circumstance is all the more notable because
all of the corpuscles at the granular layer, including the
Golgi and Cajal stellate cells, are bristly with innumerable spines. What must we infer from this? From our
point of view, this structure teaches us two things: (1)
The dislocated cells have not physiologically adapted to
the chance environment in which they live, that is, they
do not possess the characteristic spines of all of the cells
in the granular layer; (2) Because the aforementioned
dislocation does not contribute a functional adaptation,
its significance can only be to economize space, which
accounts for the dislocation itself, because there is already an excess of mitral corpuscles making it impossible to arrange all of them in a single row, and because
there is also a deficiency in the number of granules and
stellate cells in the deep molecular layer. In our opinion,
this last alternative is the most probable, and precisely
in the cat, the layers that are most proximal to the tractus, that is, the ones with the least glomeruli, granules,
and stellate cells, are the most copious in dislocated mitral cells. Nature, thus, in this case, has filled a gap and
obeyed the law of economy of space, and according to
what the research of Cajal and Lenhossék has taught
us, this is fervently shown in the retina.
The complete lack of spines, in the dislocated mitral
cells, as in the conventional mitral cells, leads us to believe
that dendrites do not need spiny appendices to carry a current. We, therefore, consider unacceptable Berkley’s conjecture, which states that the nervous surge would exclusively penetrate the collecting apparatus by means of the
cited appendices. It would be wiser to ascertain, according
to the accepted facts, that, all dendrites, even those without spines, possess receiving capability. The spines would
only expand the surface area of the entrance of the nervous stimuli, permitting a protoplasmic stem to connect
with far away nervous fibers. In this manner, the range of
action of dendrites would increase notably, and more cells
would be able to receive the nerve impulse.
The axon of the dislocated mitral cells behaves
entirely like the axon of the conventional mitral cells; it
almost always sprouts from an internal dendrite, of acriform density, confirming the law of economy of protoplasm indicated by Cajal, and proceeds toward the axis
of the bulb, getting lost in the nerve fiber layer, not
without previously having supplied collaterals for the
inter-granular plexuses.
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C. LEVINE AND A. MARCILLO
Fig. 6. Small nerve cells situated in the granular layer not far from
the epithelium. A: Cell whose axon is distributed amid the deepest
granules. B: Cell whose axon is inwardly directed, although it
branches out in the same zone. a Axon.
Cajal Cells or Descending Axon Cells
These appear in our preparations consistent with
Cajal’s description. They consist of cells that are generally found in the third peripheral area of the granular
layer. Its form is spindle shaped or triangular, and some
of its expansions, which are quite spiny, proceed toward
the peripherals, while others proceed toward the center.
The peripherals principally distribute themselves in the
deep molecular layer, occasionally reaching the mitral
corpuscle layer. The axon often proceeds from the principal peripheral expansion in accord with the law of economy of the trajectory, discovered by Cajal, it advances
undivided until reaching the deep molecular layer, in
which it branches a great deal. Ultimately, the branches
that are formed develop into varicose arborizations that
surround the mitral cell bodies and connect with the
dendritic plexus of the superficial molecular layer.
plays, and its notably dentate appearance. Nevertheless,
the Belgian scholar has not managed to impregnate the
axon, and thus, has not been able to establish the morphologic character of these nerve cells. We have been
more fortunate, being able to pursue this expansion in
many cells, and within a considerable area. As it can be
seen in Figures 7 and 5d, this axon generally proceeds
in a parallel manner extending to the layers of white
matter, or bifurcates supplying numerous branches,
finalizing within the nervous intergranular plexuses. In
the axon shown in Figure 7, the majority of the nervous
collaterals were going to these plexuses; only one branch
descends to the deep molecular layer, although it does
not pass the inferior border of this layer; in cell C, Figure 5d, the axon was very long and proceeded horizontally close to one third of a millimeter, spreading out
into various branches. In Figure 5, only a portion of its
trajectory has been reproduced.
In summary: All of the short axis–cylinder cells of the
granular layer can be classified in three groups: (1) cells
whose axon connects with the deepest granules; (2) cells
whose axon is associated with the external and medial
granules; (3) cells (Cajal cells), whose axon forms relationships in the molecular layer with the protoplasmic
plexus formed by the mitral cells, the tufted cells, and
the terminal arborization of the granules.
Do the above-mentioned short-axon cells receive
impulses from centrifugal fibers or from interbulbar
associated axons? It is actually impossible to answer
this question. The issue at hand is, anyway, very possible, because the dendrites of these cells are spiny and
they come in contact with the nervous intergranular
plexuses; but nowadays, there is no method to delimit,
between the fibers of these plexuses, the ones that are
coupled to the short axon corpuscles. If it were possible
to discover which fibers these were, then nothing would
be easier than to explain the flow of current: The nerve
Golgi Cells
Two types of these short axon corpuscles show up in
our preparations. A small corpuscle, with few expansions, that resides in the superior third of the granular
layer, often bordering the epithelial layer; and a much
more voluminous cell, with spiny expansions, housed in
the middle or inferior third of the aforementioned layer.
The small type or deeply located appears in Figure 6A,B. Spherical, triangular, or fusiform, it is characterized by the frugality of its dendrites, its small stem,
slightly larger than the thick granules, and by the varicose and minimally spiny aspect of its protoplasmic
branches. The soma is bare and seems to inhabit within
the assemblage of the granules. Its axon is fine, and proceeds in various directions in short distances, it intricately branches, generating a plexus of fine and granulose nervous branches that seem associated to the soma
and central stems of the deep granules.
The large type, or peripheral, type has been seen positively by van Gehuchten, who took notice of the extraordinary number of the peripheral dendrites that it dis-
Fig. 7. A large short-axon cell situated not far from the deep molecular layer. a: Axon. b: Row of mitral cells.
REGARDING SEVERAL POINTS OF DOUBT OF THE STRUCTURE OF THE OLFACTORY BULB
759
impulse that spreads out from the cerebral cortex or
from another part of the encephalon would go to the
soma and the dendrites of the previously cited corpuscles, from these it would propagate to the granules,
and finally, it would go up to their peripheral tufts, to
the mitral and tufted cells, with the purpose of causing
an indescribable action (Inhibition? Current loading?
Protoplasmic contractions?).
NEUROGLIA OF THE OLFACTORY BULB
The neuroglia of the olfactory bulb has been studied
by Golgi, and in particular, by van Gehuchten and Kölliker, but the descriptions given by these scholars are
rather incomplete and cannot serve to appreciate the
role that neuroglia play in the function of the bulb. The
nervous–neuroglial connection was also of interest, especially in light of the hypothesis thought up by the Cajal
brothers regarding the function of insulation of the neuroglial appendices, and in light of Weigert’s conjecture
that neuroglia is exclusively an organic filling, which is
the role it plays in the bulb, where the flow of current is
apparent, and where special zones exist that are destined for contact connections, that is the neuron–glia
connection.
The purpose of the present study is to review the
nervous–neuroglial connection. It is understood that
neuroglia may not be completely developed in newborn
animals and that its arrangement may be different in
the adult; therefore, we have impregnated olfactory
bulbs of the adult, and the 2- and 3-month-old dog and
cat. These studies have convinced us that, in fact, neuroglia, like epithelial cells, become modified in the adult
stage; because of this detail, the figures that Kölliker,
van Gehuchten, and even Golgi have drawn of the interstitial structure of the bulb weakly correspond with the
results that we have obtained; the aforementioned
authors have preferentially worked with newborn animals or postnatal animals of just a few days old. To
study the neuroglia, we have divided the bulb into the
following layers: olfactory fiber layer, glomerular layer,
molecular layer, mitral cell layer, granular layer, and
the subependymal layer or layer of epithelial cells.
Olfactory Fiber Layer
This region contains an enormous quantity of neuroglial cells, as Golgi has shown in his experiments. They
are large, stellate, or fusiform, and rest between the
strands of olfactory fibers in the thickness of this layer
preferentially close to the pia mater (Fig. 8A). The most
peripheral of these tend to take on a conical or pyramidal shape with a superficial base and an internal apex.
There are two classes of expansions (cell processes): (1)
The basal or peripheral, which are robust, granulose,
and contain intervals of plate-like crests, which penetrate into the nervous bundles to separate and isolate
the olfactory fibers. Among all of these expansions, occasionally one is found that is more robust than the
others, which terminates below the pia, amid an
enlargement. (2) The central expansion, thick at its
base, conforming into a bunch of unbranched smooth
fibers, distributed within the thickness of the molecular
layer, which pass in between the glomeruli (Fig. 8A).
This cell type most certainly belongs to neuroglial cells
Fig. 8. Neuroglial cells of the olfactory bulb of a 2-month-old cat.
A: Neuroglial cells of the nerve fiber layer. D: Interglomerular neuroglia.
B,C: Neuroglial cells whose expansions arborize within the glomerulus.
E: Neuroglial cells of the molecular layer. F: Neuroglia of the mitral cell
layer. G: Neuroglia of the deep molecular layer. H,I: Dislocated epithelial cells. J: Epithelium proper.
of Kölliker with long outgrowths, the only type that
appears to stain, as demonstrated by Cajal, using Weigert’s method. Perhaps it may have been better to consider these two as a mixed type comparable to the
description given by Terrazas (12) in the granular layer
of the cerebellum, because its internal expansions are
smooth (except at its base, which can have small plates
or collateral fins) and external varicosities supply laminar expansions.
Glomerular Layer
This region encompasses two types of neuroglia: intraglomerular cells and peri- or interglomerulares cells. The
intraglomerular cells (Fig. 8C) are robust; stellate; lie in
diverse segments of the thickness of the glomeruli; have
five, six, or more robust expansions; are bristly with
spines and branched plates; and are exclusively distributed in the glomerular territory. With a good apochromatic objective, there is evidence that these collateral
appendices constitute a kind of sponge or system of
760
C. LEVINE AND A. MARCILLO
alveoli, in which portions of nerve fibers and intraglomerular protoplasmic extensions, which should not enter
this area and form a reciprocal relationship, house
themselves. It is without a doubt that the gaps that are
seen in the intraglomerular nervous plexus that are
completely impregnated positively correspond to the
bodies of these neuroglial cells. These have been seen
but incorrectly described by Golgi, as there is no mention of their essential characteristic, which is the presence of the laminar collateral expansions.
The periglomerular cells are very robust, elongated,
and for the most part reside outside of the glomeruli,
between these and the olfactory fibers (Fig. 8B,D). Some
dwell between the glomeruli and even below the molecular layer. They possess the following: basilar expansions,
which are few in number, notably fuzzy, and destined to
separate among themselves the periglomerular nerve
cells and even the deepest strands of olfactory fibers; a
thick central stem that quickly adapts into a terminal
tuft of spongy or alveolar ramifications. This tuft penetrates into the thickness of the glomeruli sometimes
extending one, two sometimes, and even three ramifications (Fig. 8B); in other corpuscles, it can be seen crossing an interglomerular interstitium, passing the subjacent molecular layer, spilling out within, and generating
a very thick plexus with expansions of equal nature
from native neuroglial cells, or better yet, a system of
alveoli in which the fibers and cells of this molecular
layer would be partially blocked-in (Fig. 8D).
Molecular Layer
This region possesses stellate neuroglial cells of the
same variety as previously mentioned neuroglial cells,
the only difference is that they are considerably smaller,
and often their size affects their ideal stellate shape
(Fig. 8E). Some lie in the thickness of the molecular
zone; other cells inhabit the external contour of this
layer; additionally, some are in close proximity of the mitral corpuscle zone. Moreover, as indicated by van
Gehuchten, the molecular region is also where atrophic
tufts from epithelial corpuscles are located.
Mitral Cell Layer
This region scarcely contains neuroglial elements,
which are stellate and somewhat radially stretched.
They are generally in the same plane or at the borders
of the layer. The expansions, which are covered with
appendices and laminar outgrowths, are distributed in a
complex plexus in the two contiguous molecular layers;
only a few laminar expansions, which are slightly
extended, seem destined to the mitral cell interstices,
and their reciprocal contacts are avoided because of the
presence of the peripheral stems of the epithelial cells.
Granular Layer
This region encompasses two types of neuroglial corpuscles: The dislocated epithelial cells, and the short
outgrowth neuroglial corpuscles. The dislocated epithelial cells have been seen by all of the authors who have
applied Golgi’s method, and they were described in most
detail by van Gehuchten, but he, without a doubt,
worked with newborn animals and was thus unable to
observe the adult phase of these elements, which differs
in some essential features, which correspond to the first
stages of postnatal development. In the Figure 8H, we
have reproduced some of these corpuscles that were
found in the 2- to 3-month-old cat, that is to say, an age
when the neuroglial elements are completely or almost
completely formed. The cell body lies in various planes
of the layer that we are studying, it is principally
located in the central region of the granular layer, lacks
an internal prolongation, and is surrounded by a halo of
granulose appendices, which are divided into branches
that are so close to each other that it is difficult to tell
them apart, even at a high magnification.
From the peripheral portion of the layer, a thin, but
initially thick, stem sprouts out and crosses the entire
granular layer and the mitral cell layer to ultimately
end in the various molecular layers, with tufts of robust
and varicose branches (Fig. 8) that resemble webbed
feet. This endpoint, which is established in newborn animals above and between the glomeruli, seems to be
retracted in the adult, as it has been found in the external limits of the molecular layer and even in the actual
granular layer (Fig. 8); although in certain cells a defect
of impregnation cannot be excluded. The feature that is
primarily found in the dislocated epithelial adult cell is
the quantity of branched collateral expansions, destined
for the nerve fiber layer. These collateral branches often
proceed at a right angle, they integrate themselves
between the nerve fibers and nearby granular expansions in the aforementioned plexuses, and give off a
spongy frame, similar the one described by Cajal in the
molecular layer of the cerebellum. From time to time,
and generally corresponding to the central limit of a
given group of granules, the appendices multiply and
lengthen, generating a sort of rippled tuft whose appendices run within the aforementioned limit. Additionally,
other appendices, which are more or less smooth and radial, pass in between the cell bodies of the granules to
impede contact between them. Each epithelial cell can
form two or more ornamental borders of this type, the
latter of which inhabits the internal molecular layer.
The stems of the epithelial cells, are smooth as they
pass through the granular cells, and expand their ramifications in the nervous plexuses; this is done in such a
way that the vast majority of the expansions seem destined to fill the existent intervals between the infinite
protoplasmic and unmedullated nervous branches that
rest in the stratum of the granular and molecular layers.
The other cell type corresponds to the neuroglial category of short hair-like radiations: These preferentially
live in the intergranular layer (Fig. 8G) and when its
expansions pass through the granules, they are more
smooth and more moderately branched than when they
integrate themselves between the prolongations of the
granules.
Subependymal Layer or Layer of
Epithelial Cells
In mammals, below the ependyma, exists a thick zone
exclusively inhabited by the bodies of the epithelial cells.
These exhibit an ovoid body, which is either smooth or
contains small outgrowths, a central expansion with
some crests and accommodation protuberances, and a
peripheral prolongation, which is initially curved, to
accommodate the soma of analogous corpuscles, and
REGARDING SEVERAL POINTS OF DOUBT OF THE STRUCTURE OF THE OLFACTORY BULB
which, once it arrives at the granular layer, behaves in
the same manner as the soma of the dislocated epithelial
cells (Fig. 8J). In summary, the presence of the central
expansion extended to the ependyma, the low number of
outgrowths of the soma, peripheral stem structure, and
subependymal disposition, are features that, at first
glance, allow the distinction between these and the epithelial dislocated cells. Additionally, in the adult dog
and cat, the thick, deep strands of myelinated nerve
fibers contain stellate cells with smooth and long radiations, a finding that is equivalent to findings in man.
The findings regarding neuroglial disposition that we
have just described seem to favor the opinion of the
brothers Cajal more so than of Weigert; however, with
present-day science, it is impossible to formulate a definite tenet. We see, in fact, in the area where the olfactory fibers lie, the quantity of neuroglial fibers is enormous, existing to impede the contacts between the
fibers, there is a multitude of crests and collateral
appendices of accommodation. The same occurs in the
glomeruli, interglomerular spaces, and molecular layers.
The contacts between the innumerable dendritic expansions that are concentrated in these plexuses and the
unmedullated nervous fibers, in a similar manner as the
aforementioned neuroglial intersticial plates, consisting,
as previously described, by a sort of sponge that groups
together these ramifications. Briefly, the insulating neuroglia is present in all of the areas of the bulb where
conductive fibers are, and, where the risk of an uncontrolled diffusion of the olfactory impulse is greater. Neuroglia, therefore, has in this case, the task of channeling
currents, isolating from one another all of the expansions that pertain to systems of independent conduction.
On the other hand, the corpuscles of long outgrowths
would dominate at the regions formed exclusively by
medullated tubes and where the aforementioned channeling is not necessary.
DO NERVE FIBERS OF BULBAR ORIGIN THAT
PENETRATE INTO THE GLOMERULI EXIST?
The doctrine of dynamic polarization, created by Cajal,
based on the way the sensory nerves terminate, has a
great line of reasoning in the olfactory bulb, according to
van Gehuchten, His, Edinger, Lenhossék, Retzius, and
Kölliker. The fundamental fact, favorable to said doctrine, is the following: In the glomeruli, there is exclusive branching by the olfactory nerve fibers without
passing further within the structure, and only the protoplasmic expansions of the mitral and tufted cells arrive
to gather the olfactory impulse deposited in these territories by the fibers. Because no nerve fiber, collateral or
terminal, coming from the torso of the olfactory bulb
penetrates the glomerular area, there is no other
recourse than to allow transmission by contact between
the olfactory fibers and the aforementioned protoplasmic
appendices. The asserted facts, and the explanation
founded in them, are so very clear and easy to demonstrate, that all authors have given them credence, less
those compromised by the defense of personal theories.
Consequently, is it no surprise to see that Golgi and his
disciple A. Monti are still adamant that the protoplasmic
expansions that penetrate into the glomeruli, do not
serve for impulse conduction, and the olfactory current
is delivered exclusively by long axons and nervous col-
761
laterals. In fact, Golgi (13), in a minimally impartial,
critical article, reviewing new work on the olfactory
bulb, recalls the existence of recurrent nervous collaterals, which sprout from the axon of tufted corpuscles and
from other cells deep in the olfactory tract, have their
endpoints in the glomeruli, where they would anastomose with the olfactory fibers. These collaterals would
not have been, according to the Italian scholar, stained
in Cajal’s preparations. A. Monti (14), a devoted disciple
of Golgi, in a brief composition on the subject, refutes
the contact theory, asserting to have seen outgrowths
from the axons of small paint brush-like cells (inferior
tufted Cajal cells) arrive at the recurrent glomerular collaterals. These collaterals form a scaffold within the glomerulus, which continues peripherally with the olfactory
fibers.
With such insistence, in the presence of a great determination to defend at any cost, a doctrine that has been
unanimously rejected by the most notable histologists,
we would simply be able to refrain from the subject, and
state only that we have never managed to see the
referred to recurrent fibers, despite having examined
some hundreds of high-quality preparations, in which,
uncountable olfactory fibers showed up completely
impregnated. Moreover, as we cannot but assume that
Golgi and Monti proceed with good faith, and they have
positively seen possible elements that would induce
them to ponder the existence of the aforementioned connection, we have tried to find the fibers that these scholars have identified as nerves and recurrent fibers. These
fibers are varied and of diverse nature. They are as
follows:
Collateral Fibers From Inferior Tufted Cells
In fact, there exists, as we have said previously, certain recurrent collaterals of tufted cells, but these fibers
arborize exclusively between the glomeruli and never
within them. An analysis of fine slices in alcohol or in
xylol to avoid such excessive transparency that the balsam or the Damar resin imparts onto the glomeruli,
allows the true topography of the aforementioned collaterals to be distinguished.
Axon collaterals of Mitral Cells
These can go up to the molecular layer, but they never
enter the glomeruli nor do they reach the border of the
glomerular layer.
Terminal Tufts of the Epithelial Cells
In newborn or postnatal mammals of just a few days
old, radial fibers are sometimes found that end on or
within the glomeruli by means of a tuft of strongly varicose branches. These fibers, when thin or do not stain
completely until its arrival at its cell of origin, could
give rise to errors of interpretation.
Fine Dendritic Appendices Emanating From
Dislocated Mitral Cells and From Those in
Their Usual Position
Also the aforementioned stems, which branch out frugally within the glomeruli, could appear, upon a superficial examination, like centrifugal nerve fibers (Fig. 5g,h).
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C. LEVINE AND A. MARCILLO
In summary, a nerve fiber that originates in the bulb,
or other major center, would never end up within the
glomeruli. Although a comparable termination is occasionally found, we have gone through hundreds of preparations, asking: ‘‘How does this finding oppose the contact theory and the doctrine of dynamic polarization?’’
Within this doctrine, these findings are easily explained
by simply visualizing that certain tufted cells propagate
electric current in two modes, directly and indirectly.
That is, directly, by means of the axon, and indirectly, or
through its collaterals, which at the level of the glomeruli, enters into a contact relationship with the dendritic
tufts of other corpuscles of the same type.
Golgi and Monti’s doctrine demonstrates its weak
foundation by not giving any importance to the most
essential facts of the structure of the bulb. To believe in
these scholars would lead to the following outcome: (1)
that millions of mitral cell, medial and inferior tufted
cell, dendritic expansions end in the glomeruli in intimate contact with the olfactory fibers, and are only an
adornment with no other function than to serve as an
eternal enigma for neurologists. Moreover, the wellknown mitral cells would not serve a function, despite
generating the largest fibers from the external root of
the olfactory nerve, because—as Kölliker points out—
with Golgi’s doctrine they would be excluded of all olfactory conductive function. (2) Millions of olfactory fibers
come to an end within the glomeruli and then the rare
and scarce recurrent Golgi and Monti fibers emerge
from the glomeruli (because it is impossible from all
points of view that they could have found many fibers
that appeared to have an endpoint in the glomeruli),
resulting in the current arriving at the olfactory mucosa,
being discontinuous at the borders of the olfactory
apparatus.
Let us point out, that the aforementioned recurrent
fibers are completely missing in the inferior vertebrates,
in which, as demonstrated by the brothers Cajal, Calleja, Edinger, and others, glomeruli exist and represent
the only juncture between the olfactory fibers and the
protoplasmic tufts of the bulbar cells; which reveals, the
great importance of the nervous–protoplasmic connection
that occurs in the glomeruli, present in all vertebrates.
In conclusion, Golgi and Monti’s opinion does not have
concrete facts to support it, but false interpretations. In
order for this doctrine to be formally discussed, it would
be necessary that these scholars get preparations where
these two findings appear: (1) the existence of glomeruli
in a vertebrate, where no dendritic expansion that
comes from a mitral or tufted cell, is penetrating the glomeruli; (2) the presence of olfactory fibers that, piercing
the borders of the glomeruli, continue without interruption by way of axons or nervous collaterals of tufted
cells. Without trying to be prophetic, we believe that we
are not mistaken when predicting that neither Golgi nor
his disciples would have the opportunity to contradict
the referred facts.
Recently Manouelian (15), while defending Duval’s ingenious theory concerning the nervi nervorum, believed to
have found centrifugal nerve fibers in the thickness of the
olfactory bulb, possibly coming from the brain, and that
terminated in the glomerulus. By way of these centrifugal
fibers, which Manouelian compares to the ones found by
Cajal in the retina, the nerve centers would act on the
nervous–dendritic articulation of the glomeruli, regulating the intensity of, or facilitating the flow of current.
We will not refute Manouelian’s assertion, which has
the merit to fit well within the existing doctrine about
the functionality of the senses; but, we must confess that
we have not managed to come across the aforementioned
fibers. Could it be that the aforementioned scholar has
mistaken fine dendrites of dislocated mitral cells for
nerve fibers, like, for example, the ones that we have
depicted in Figure 5g? To pursue this issue, it would be
necessary to not only consider the description and drawings given by this author, but also examine his preparations and compare them to ours. Therefore, we reserve
our opinion on this point, in anticipation of new reports.
ACKNOWLEDGMENTS
Excerpts from this work was previously presented in a
poster entitled ‘‘The origin of the first cranial nerve: The
fila olfactoria according to Santiago Ramón y Cajal and
T. Blanes’’ by C.L. at the 2006 International Meeting of
the Cajal Club in Stockholm, Sweden, at The Nobel Forum, Karolinska Institutet in celebration of the Centennial Anniversary of the Nobel Prize jointly awarded to
Santiago Ramón y Cajal and Camillo Golgi in Physiology
or Medicine (1906) for their work in the field of neuroscience. Funding for attendance at the International
Meeting of the Cajal Club was provided to C.L. by the
International Brain Research Organization (IBRO).
Illustrations by T. Blanes have been digitally enhanced
for color and quality. Original Title: Sobre algunos puntos
dudosos de la estructura del bulbo olfatorio. T. Blanes,
Revista Trimestral Micrográfica 3, 99–127 (1898).
LITERATURE CITED
1. Golgi. Sulla fina struttura dei Bulbi olfatorii. Reggio-Emilia,
1875.
2. Cajal. Origen y terminación de las fibras nerviosas olfatorias.
Diciembre, 1890. Barcelona.
3. P.Ramón. Estructura de los bulbos ópticos de las aves. Gaz.
Sanit. De Barcelona. Julio 1890. El encéfalo de los reptiles, Septiembre de 1891. Barcelona.
4. Van Gehuchten y Martı́n. Le bulbe olfatif de quelques mammiferes. La Cellule, t. VIII, 2 fasc. 1891.
5. Retzius. Biol. Untersuchungen Neue Folge, 1892.
6. C.Calleja. La región olfatoria del cerebro. Madrid, 1893.
7. Kölliker. Lehrbuch del Gewebelehre, 6 Aufl. Bd. II, 1896.
8. Cajal. El sistema nervioso de los vertebrados. Fasci. I, 1897.
9. A.Hill. Notes on granules. Brain. Vol. 77 y 78. 1897.
10. Mathias Duval. L’amoeboisme du systeme nerveux. La théorie
histologique du sommeil. Les nervi nervorum. Revue Scientifique, 12 Mars., 1898.
11. Manouelian. Societé Biologie, 19 Fevr. 1898.
12. Terrazas. Notas sobre la neuroglia del cerebelo, etc. Rev. trimestral micrográfica. Tomo 11, 1897.
13. Golgi. Ergebnisse der Anatomie und Entwickelungsgeschichte,
11 Band, 1892. Articulo Nervensystem. Wiesbaden, 1893.
14. Monti. Sulla fina Anatomia del Bulbo olfattorio. Fatti vecchi e
nuovi che contradicono alla teroria dei Neuroni. Paris, 1895.
15. Manouelian. Societé de Biologie, 19 fevrier 1898. Also see L’anne
psychologique, Paris, 1898. p. 447, and Deyber’s Thesis. Etat
actuel de la question de l’amoeboidisme. Steinheil. Paris, 1898.
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