\ \ I I R . /OOICK.ISI, ->:."!Il-S'ifi (19<">r.).
FINE STRUCTURE OF THE NERVOUS SYSTEM OF HYDRA
THOMAS L. LFNTZ AND RI-SSFLI. J. BARRNF.TT
Dept. of Anatomy, School of Medicine, Yale University, Xew Haven, Conn.
SV.NOPSIS. Fine structural details of the cells and processes of the h\dra nenous
sjstem are reported in this paper. Ganglion cells are small bipolar or nmltipolar
cells situated above the muscular processes of epitheliomusiular cells. An elaborate
Colgi apparatus consisting of parallel lamellae anil small and large vesicles is present
in these cells. Some cells are poor in ribosomes while others contain numerous free
ribosomes. In the ribosome-rich cells, small membranous microHibules originating
from the nuclear envelope extend into the cuoplasm and neurites. The neurites also
contain vesicles and mitochondria and terminate at the bases of cnidoblasts and on
the muscular processes of epitheliomuscular cells. Specialized synapses were not
observed.
A second cell t>pe contains man) membrane-bounded dense granules, 1000 A in diameter, and these are considered to be neurosecretory cells. Xeurosecretory granules
on cnidoblasts and epitheliomuscular cells. Sensoi) cells are small elongated cells
originate in the Golgi apparatus and are abundant in neurites which also terminate
situated between the apical surfaces of epithelial and digestive cells. These cells are
characterized by an apical specialization which appears to be a modified cilium.
Neurosensory cells were also observed. The intimate connection of the nervous s)stem
with cnidoblasts suggests a role in nematocjst discharge. The finding of neurosecretory
material supports the hypothesis that the neural control of regeneration in hydra
is regulated by material released at nerve endings.
A cell type has not been identified in
hydra at a fine structural level that bears
strict resemblance to mammalian neurons
(Hess, et al., 1957; Chapman and Tilney,
1959; Slautterback and Fawcett, 1959;
Wood, 1959; Hess, 1961), but the existence
of a nervous system in hydra cannot be
denied in view of the accumulated evidences from morphological, physiological,
and histochemical studies. This paper describes the fine structural details of cells
and processes identified as comprising the
hydra nervous system, as defined in earlier
morphological and histochemical studies.
Many previously unreported morphological
details of these cells and processes have become apparent, the most significant of
which is the finding of what is presumed
to be neurosecretory material.
MATERIALS AND METHODS
Hydra littoralis were maintained in culture according to the method of Loomis
and Lenhoff (1956). These animals were
either fixed for 1 hour in cold 1% buffered
osmium tetroxide (pH 7.2) containing 0.4
M sucrose (Caulfield, 1957), or were fixed
in cold 4% buffered glutaraldehyde (Saba-
tini et al., 1963) prior to a second fixation
in osmium tetroxide. The fixed tissues
were dehydrated with graded concentrations of ethanol and embedded in Maraglas
(Freeman and Spurlock, 1962). Thin sections were cut on a Porter-Blum microtome
and examined with an RCA EMU 3F electron microscope. Most sections were stained
with lead hydroxide (Feldman, 1962) prior
to examination. In some cases, nerve cells
were identified with the light microscope
in 1 jt thick sections and examined with
the electron microscope in adjacent thin
sections.
OBSERVATIONS
During the study of the several cell types
in different regions of hydra, elements of
a well-developed, complicated, and diffusely
organized nervous system were found. Because this system is most concentrated in
the distal body regions, the present observations were largely gathered from study of
this area. Several cell types and their neurites (processes) comprise the nervous system: ganglion, neurosecretory, and sensory
cells.
Small, elongated ganglion cells with one
(341)
342
THOMAS L. LENT/, AND RUSSELL J. BARRNETT
or more neurites arc situated at the bases
ol epithelioniuscular cells just above their
muscular processes (Fig. 1). The nuclei of
these cells are small and oval, bounded by
a nuclear envelope that contains numerous
pores (Fig. 2, 4, 5, 5 insert). Nucleoli are
not prominent. The cytoplasm of ganglion
cells shows some variations in regard to the
ribosomal population. Some cells (Fig. 4,
5) contain numerous ribosomes lying free
in the cytoplasm, unassociated with membranous components of the endoplasmic
reticulum. Ribosomes also occur in the
neurites (Fig. 5) and therefore nothing
comparable to an axon hillock is present.
Other cells, equal or slightly fewer in number, have a similar shape and position, but
few ribosomes (Fig. 1-3). Profiles of
smooth- and rough-surfaced endoplasmic
reticulum are present in both cell types
(Fig. 1, 4, 5) but are not a prominent feature
of either. The plasma membrane of the
ganglion cells is irregular with numerous
small crests and indentations (Fig. 3, 5),
and no specialized regions comparable to
synapses on the soma of the ganglion cell
were seen. No extraneous coat or basement
membrane covers the plasma membrane
(Fig. 1, 3, 5).
Two other morphological features of the
cytoplasm of these cells are prominent. The
first is the occurrence of microtubules only
in the ribosome-rich ganglion cell (Fig. 4,
5, 5 insert). These structures, which require very thin sections for their resolution,
can be clearly delineated from profiles of
endoplasmic reticulum. T h e microtubules
are composed ot a membranous envelope
approximately 40 A thick enclosing a relatively clear space 120 A in diameter. These
structures are situated in the cytoplasm in
a direction parallel to the long axis of the
neuron and extend out into the neurites
(Fig. 5, 13). At their central end they appear to curve and to come into close proximity to nuclear pores (Fig. 4, arrows; 6).
T h e other prominent feature of the cytoplasm common to both types of cells, but
more pronounced in the ribosome-poor
cells, is an elaborate Golgi apparatus (Fig.
2-4: GA). In fact, some of the cells have
two or three distinctly separated Golgi re-
gions (Fig. 2, 3). This organelle is usually
situated between the nucleus and a neurite.
When it occurs in this morphological situation, its long axis is parallel to the long
axis of the cell, extending from the nuclear
region to the base of a neurite (Fig. 2, 3).
When the organelle is unassociated with a
neurite, its long axis is perpendicular to
the long axis of the cell (Fig. 2). In some
instances, the Golgi apparatus is located
entirely within the neurite base (Fig. 3, 14).
Each Golgi apparatus is characteristically
composed of flattened, parallel stacks of
membrane-bounded lamellae and small vesicles (Fig. 2, 3). In these organelles, the
small vesicles appear to arise by a pinchingoff process from the ends of the lamellar
stacks. These small vesicles contain a material of light and homogeneous density.
Mitochondria showing no unusual fine
structural features are scattered irregularly
in the hyaloplasm of the perikaryon of
ganglion cells (Fig. 1, 4). However, they
regularly occur in relation to the elaborate
Golgi apparatus; sometimes occurring parallel to the stacks of lamellae, but more
often occurring in relation to the Golgi
lamellae and small vesicles (Fig. 3, 14).
Neurites of these cells extend from the
perikaryon between other cell types (Fig. 1;
5, P). In most cases these processes are so
tortuous that at best they can be followed
for only 5 to 10 p., and are of irregular diameter, containing bulbous enlargements
in some areas. Neurites of ribosome-rich
cells contain microtubules (Fig. 5, MT)
and at several loci these appear to approach
the plasma membrane. In ribosome-poor
cells, small as well as a few larger vesicles
(V) contain a material of low density (Fig.
3). Mitochondria (M) are interspersed
among these organelles. As previously reported for other coelenterates (Horridge
and Mackay, 1962), nothing comparable
to a myelin sheath is found. However, the
perikaryon of the ganglion cells is almost
completely enclosed by other cells, presumably epitheliomuscular in type (Fig.
3). Neurites often are surrounded by other
cell types, but sometimes are found in intercellular spaces unassociated with other
cells (Fig. 5).
NKRVK CKI.LS IN Hydra
Terminations of neurites were difficult
to recognize, or indeed find because of the
tortuosity of the fibers. However, it appears
that at least some of the fibers end at the
base of cnidoblasts (Fig. 7, Cb) and near
the processes of some epitheliomuscular
cells. The ending appears as a bulbous
cluster containing a few vesicles and small
mitochondria. No morphological specializations of surface contacts comparable to
synaptic regions in higher forms are present.
Some similar cells contain many membrane-bounded dense granules; these cells
are presumed to be neurosecretory cells (Fig.
8-10). Neurosecretory cells are similar to
ganglion cells in size, shape, and position,
in relation to epitheliomuscular cells, and
in cytoplasmic contents except for their
membrane-bounded dense granules which
are about 1000 A in diameter. The granules
(NG) are present in the cytoplasm of the
perikaryon (Fig. 8), within processes (Fig.
12, 13) and often occur in close relationship
to elements of the Golgi apparatus (F"ig.
9-11). Some are located in the dilated ends
of lamellae and vesicles of the Golgi (Fig.
11) which is more complex and larger than
those in ganglion cells. In addition, a
diffusely organized, moderately dense material occurs within the hyaloplasm and
is usually situated within or adjacent to
the Golgi apparatus, sometimes surrounded
by small vesicles (Fig. 9, 10).
Neurosecretory cells invariably contain
many ribosomes, while elements of an endoplasmic reticulum are not prominent (Fig.
10). Microtubules are present but not numerous. Their nuclei are oval, irregular
in shape, contain one or more indentations,
and one or more nucleoli.
The neurites of the neurosecretory cells
also have a complicated and irregular
course. Dense granules, ribosomes, microtubules, and occasionally mitochondria
(Fig. 12, 13) are contained within neurites
which terminate adjacent to muscular
processes, cnidoblasts, or the intercellular
spaces. Dense granules, presumably neurosecretory in nature, are concentrated at the
terminations of neurites, and at these sites
are contained within dilated smooth-surfaced vesicles which sometimes approximate
343
the surface membrane of the neurite (Fig.
13). In addition, empty dilated vesicles
also occupy the same regions (Fig. 12, 13).
Large granules are not observed in the intercellular spaces, although neurites are
usually surrounded by large accumulations
of less dense extracellular granules, 300 A
in diameter (Fig. 13, 16). The small granules also occur in large numbers in the
mesoglea and in intercellular spaces between the basal portions of cells of the
epidermis and, to a lesser extent, gastrodermis.
Nerve cells of the base of the animal do
not strictly resemble those cells just described. They contain no microtubules and
ribosomes are not abundant. A Golgi apparatus is present but is often confined to
the base of a process. Although granules
are rarely seen in the perikaryon of these
cells, small dense granules 200-300 A in
diameter are regularly found either within
the dilated ends of Golgi cisternae or small
vesicles or as membrane-bounded accumulations within the cytoplasm of the process
(Fig. 14).
Sensory cells are small and elongated,
situated between and near the apical surface of epithelial or digestive cells, and
contain an elaborate apical specialization
(Fig. 15). Only a small portion of the apex
of the cell reaches the surface, and this is
indented to form an apical collar (Fig. 15;
16, AC). From the base of the indentation
a process arises that contains a single modified cilium (C). That portion of the cilium
contained in the process has nine pairs of
peripheral fibers which in longitudinal section show a dense core, but the center of
the cilium is occupied by more than the
usual pair of fibers (Fig. 16). Below the
base of the modified cilium the fibers merge
with dense material, presumably modified
basal body. From the base of this dense
material, small (about the diameter of
microtubules) dense filaments or rootlets
(R) splay out into the apical cytoplasm.
Just below the rootlets the cytoplasm contains many mitochondria and small smoothsurfaced vesicles (Fig. 15). An elaborate
Golgi apparatus occurs between the apical
specialization and the nucleus. The apical
344
THOMAS L. LENTZ AND RUSSKLL J. BARRNETT
portion of the cell also contains many
microtubules parallel to the long axis of the
cell (Fig. 15). The opposite pole of the cell
is drawn into a blunt cytoplasmic process
which terminates in the vicinity of a ganglion cell.
In several instances one process of a
deeply situated ganglion cell resembled the
apex of a sensory cell (see Jha, 1965). From
the primary process containing mitochondria a thin secondary process arises that
contains a single cilium which protrudes
between cells to reach the surface (Fig. 17).
DISCUSSION
It is perhaps surprising that previous
investigators have been unable to identify
any component of the hydra nervous system
with the electron microscope. Previous
studies provided ample evidence for the
existence of a nervous system. However,
because hydra possesses one of the most
primitive metazoan nervous systems, it is
doubtful if the morphological criteria for
the identification of mammalian neurons
can be applied to their nervous system.
Furthermore, nerve cells are not as numerous as other cell types, and thin sections
obtained through both cell body and processes are fortuitous.
Certain criteria based on light microscopic observations may be used in identifying the nervous system at a fine-structural
level. The most important of these characteristics are position and shape. Neurons
(except lor certain sensory cells which are
situated between the apices of epithelial
cells) lie above the muscular processes of
the epitheliomuscular and digestive cells
and are most abundant in the hypostome
and base. They are seldom observed in the
gastrodermis. Neurons are bipolar or multipolar, their neurites extending above the
mesoglea and bases of epidermal and digestive cells and terminating near other cell
types. Four of the cell types in hydra—
cnidoblasts, epitheliomuscular, digestive,
and gland cells—are easily distinguished
from neurons on the basis of their characteristic cUoplasmic specializations. I'ndifterentiated and differentiating interstitial
cells, which have the same position in lela
tion to the epitheliomuscular cells, provide
the greatest potential source of confusion.
These cells, however, do not possess long
processes and are most abundant in the
growth region. T h e cytoplasm of interstitial cells may be recognized by a paucity
of organelles and a plethora of ribosomes.
Neurons contain fewer ribosomes but a
well developed Golgi apparatus.
Neurons are classified as: (1) ganglion,
(2) sensory, and (3) neurosecretory cells.
Ganglion cells typically contain either few
or numerous ribosomes and an elaborate
Golgi apparatus which is polari/.ed in relation to the neurites. Mitochondria are
always positioned in relation to the Golgi.
Numerous small vesicles with electronlucent contents appear to arise from the
Golgi lamellae and also occur in the processes. Microtubules are present only in
the ribosome-rich cells. Two similar cell
types can be distinguished, one containing
liuosoir.es and microtubules, the other not;
otherwise the two cell types are quite similar. If ganglion cells differentiate from interstitial cells, it is entirely possible that
the two types described represent one cell
line in different stages of development.
Since the hydra is continually producing
new cells that move distally and proximally
as they differentiate, the ribosome-rich cell
could be the less mature. Alternatively,
the morphological results could be interpreted as the same cell type in two different
functional states.
Sensory cells ol hydra are interspersed
between the apices of other cells in the
epidermis and gastrodermis, and possess a
specialized apex containing a modified
cilium. An elaborate Golgi apparatus is
situated beneath the cilium in the supranuclear part of the cell, and microtubules
are abundant. This cell was the only one
found at the outer or inner surface of hydra
that at all conforms in structure to a possible receptor, but it is not known what
sensory modality it receives. Since the hydra is sensitive to light and one of the two
basic types of photoreceptor found in all
animals is of ciliary origin, it is tempting
to suggest a photoreceptor function for this
structure. However, no photopigment was
NFRVF. CF.I.IJ IN
recognized, and a photoreceptor in the
hydromedusan Polyorchis penicilltitus is far
more elaborate (Eakin and Westfall, 1962).
The apical portion of this cell suggests a
neuronal character, and the basal process
of the cell extends toward ganglion cells.
On occasion, sensory cells are found closer
to the base of the epitheliomuscular cells;
in these the modified cilium projects from
one process to gain the surtace. This cell
corresponds to the neurosensory cell described by Hadzi (1909) and McConnell
(1932). Its sensory function too remains
unknown.
Neurosecretory cells are easily recognized
by their content of dense membrane-bounded granules, but also because they do not
synapse with other neurons or effector cells.
These observations are in agreement with
the established definition (Scharrer, 1962)
of neurosecretory cells, in hydra the granule-laden cells terminate between or on
other cell types, and in some cases vesicles
containing neurosecretory material appear
to be emptying into the extracellular
spaces. In this regard, the intercellular
spaces of hydra might correspond to the
circulatory system of higher animals.
The granules appear to be elaborated by
the Golgi apparatus in these cells, as has
been suggested for all other neurosecretory
cells (Bern, et al., 1962). The population of
membrane-bounded dense granules is most
abundant near the Golgi apparatus, frequently in the dilated ends of Golgi lamellae, and also at the ends of the processes.
Only a few granules are present in the
perikaryon of these cells, and microtubules
are especially abundant in the processes.
Other neurons, presumably neurosecretory
in function and possessing small granules,
are present in the base.
Granule content aside, ganglion and neurosecretory cells have certain similarities.
Cells of both types are similar in size and
shape, and possess an elaborate Golgi apparatus, ribosomes, and microtubules. In
fact, ganglion cells may have a neurosecretory function since they contain many small
vesicles in the Golgi region as well as in
the processes. Thus, it could be interpreted that a different neurosecretory ma-
Hydra
315
terial is present in the vesicles of the ganglion cells from that present in the dense
granules of the neurosecretory cells. In
addition, it is possible that the neurosecretory cells and ganglion cells represent the
same cell line in different stages of function
and differentiation.
All neural elements except for the ribosome-poor ganglion cells contain microtubules. This finding is not diagnostic of
neural elements, since similar microtubules
also occur in other cell types of the hydra
(Slautterback, 1963; Lentz, unpublished observations). The function of these minute
structures is not known, but it may be significant that they are present in both perikaryon and neurite. One end at least of
some microtubules appears to come in close
relationship with nuclear pores, and this
might suggest a role in nucleo-cytoplasmic
relationships. At the other extremity microtubules appear to come in relation to the
plasma membrane, especially that of the
processes. Slautterback (1963) has suggested these structures could play a role in
transport of water or ions.
Neurites are tortuous and the terminations difficult to identify. They contain
small vesicles, mitochondria, granules, and
microtubules, depending on the cell type.
The only information bearing on the controversy as to whether the nervous system
is synaptic or continuous, or on whether or
not conduction can occur equally well in
all directions, are the present observations
that the nervous system is composed of
separate neurons and that no typical specialized synapses were observed. Instead,
terminations of neurites consist of bulbous
enlargements adjacent to other cell types.
Thus, it is possible that impulses could pass
in either direction at abutments of neuronal elements for some cells. The finding
of neurosecretory material suggests polarization of function at least for these cells.
Epitheliomuscular cells and especially
cnidoblasts have been observed to be in
contact with elements of the nervous system (see: Lentz and Barrnett, 1961). With
the electron microscope this relationship is
even more intimate than supposed, since
processes of ganglion and neurosecretory
3-16
THOMAS L. LENTZ AND RUSSELL J. BARRNETI
cells are seen in close association with the
base of cnidoblasts and epitheliomuscular
cells. Moreover, the granule-laden neurosecretory cell terminations abut on cnidoblasts, supporting the suggestion (Lent/,
and Barrnett, 1962) that the nervous system
plays a significant role in nematocyst discharge.
It was previously shown that the nervous
system plays a key role in growth, differentiation, and acquisition of normal form
in regenerating hydra and if inhibited, regeneration does not occur (Lentz and Barrnett, 1963). It was, therefore, suggested
that control of these processes was mediated
by neurosecretory material released by
nerve endings. In addition, Burnett (1961,
1962) has presented evidence for the existence of growth-controlling substances, and
these also may be a function of the nervous
system. The present studies have established that the hypothesized neurosecretion
has a morphological basis, since two different types of neurosecretory material were
identified; possibly a third emanates from
the vesicles of ganglion cells. Presumably,
one or all of these structures contain the
substances which play a key role in regulating growth, differentiation, and the anatomical form of this animal.
ACKNOWLEDGMENTS
This work was supported by N.l.H.
grants AM-03688 and TICA-5055. It represents part ot the material submitted in
fulfillment of the thesis requirement of the
first author for the M.D. degree, Yale University School of Medicine.
REFERENCES
Bern, H. A., R. S. Nishioka, and I. R. Hagaclorn.
J962. Neurosecretory granules and the organelles
of neurosecretory cells, p. 21-34. In H. Heller
and R. B. Clark, (eds.), Neurosecretion. Mem.
Soc. Endocrinol. No. 12. Academic Press, Inc.,
New York.
Burnett, A. L. 1961. The growth process in hydra.
J. Exptl. Zool. 146:21-84.
Burnett, A. L. 1962. The maintenance of form in
hydra, p. 27-">2. In I). Rudnick. (ed.). Regeneration. Ronald Press, New York.
( aulfield. J B 1957 Effects of \ar\ing the \ehicle
for osmium tetroxide in tissue fixation. J Biopin- Riorhem. C\tol. 3:827-833.
Chapman, C... and I.. "1 ilney. 1959. Cytological
studies of the nematocysts of hydra. I. Desmosomes, isorhizas, cnidocils, and supporting structures. J. Biophys. Biochem. Cytol. 5:69-78.
Eakin, R. M., and J. A. Westfall. 1962. Fine structure of photoreceptors in the hydromedusan,
Polyorchis penicillatus. Proc. Nat. Acad. Sci. U. S.
48:826-833.
Feldman, D. G. 1962. A method of staining thin
sections with lead hydroxide for precipitate-free
sections. J. Cell Biol. 15:592-595.
Freeman, J. A., and B. O. Spurlock. 1962. A new
epoxy embedment for electron microscopy. J.
Cell Biol. 13:437-443.
Hadzi, J. 1909. Ober das Nervensystem von Hydra.
Arb. Zool. Inst. Wien 17:227-268.
Hess, A. 1961. The fine structure of cells in hydra.
p. 1-49. In H. M. LenhofE and W. F. Loomis,
(eds.), The biology of hydra and of some other
coelenterates. Univ. Miami Press, Coral Gables.
Hess, A., A. I. Cohen, and E. A. Robson. 1957. Observations on the structure of hydra as seen with
the electron and light microscopes. Quart. J.
Microscop. Sci. 98:315-326.
Horridge, G. A., and B. Mackay. 1962. Naked axons
and symmetrical synapses in coelenterates. Quart.
J. Microstop. Sci. !03-Ml-541.
Jha, R. K. 1965. The nerve elements in siiveistained preparations of Cordylophora. Am. Zoologist 5:431-438.
Lentz, T. L., and R. J. Barrnett. 1961. Enzyme
histochemistry of hydra. J. Exptl. Zool. 147:
125-150.
Lentz, T. L., and R. J. Barrnett. 1962. The effect
of enzyme substrates and pharmacological agents
on nematocyst discharge. J. Exptl. Zool. 149:
33-38.
Lentz, T. L., and R. J. Barrnett. 1963. The role of
the nervous system in regenerating hydra: The
effect of neuropharmacological agents. ). Exptl.
Zool. 154:305-328.
Loomis, W. F., and H. M. Lenhoff. 1956. Growth
and sexual differentiation of hydra in mass culture. J. Exptl. Zool. 132:555-568.
McConnell, C. H. 1932. The development ol the
ectodennal nerve net in the buds of hydra. Quart.
J. Microscop. Sci. 75:495-509.
Sabatini, D. D., K. Bensch, and R. J. Barrnett. 1963.
The preservation of cellular ultrastructure and
enzymatic activity by aldehyde fixation. J. Cell
Biol. 17:19-58.
Scharrer, E. 1962. Concluding remarks, p. 421-424.
In H. Heller and R. B. Clark, (eds.), Neurosecrelion. Academic Press, Inc., New York and
London.
Slautterback, D. B. 1963. Cytoplasmic microtubules.
I. Hydra. J. Cell Biol. 18:367-388.
Slautterback, D. B.. and D. W. Fawcett. 1939. The
development of the cnidoblasts of hydra. An
electron microscope study of cell differentiation.
J. Bioph\s. Biochem. Cstol. 5:441-452.
Wood, R. L. 1959. Intercellular attainment in
\ I R \ I . GILLS IN
the epithelium ol India as ie\eak'd l)\ electron
microscopy, f. Biophys. Biochem. Gytol. 6:3433J2.
EXPLANATION OF FIGURES
PLATE 1
FIG. 1. Small ganglion cell situated adjacent to
the muscular processes (MP) of epitheliomuscular
cells. The perikaryon contains mitochondria and a
lew smooth membranous cisternae. Few ribosomes
are present. A Golgi apparatus (GA) is located in
the base of a process (P). X 18,000
FIG. 2. Ribosome-poor ganglion cell containing
three Golgi complexes (GA). Those situated at the
bases of a process (P) are oriented in a direction
parallel to the long axis of the cell. X 50,000
347
Ilydia
FIG. 7 (upper right). Two neurites (P) of a ribosome-poor ganglion cell situated at the base of a
cnidoblast (Gb). The neurites contain small mitochondria and a few \esicles. A specialized synaptic
complex is not present. Small dense granules are
present in the intercellular spaces surrounding the
neurites. X 24.000
FIG. 8 (center). Xeurosecretory cell containing
dense membrane-bound granules (XG) in the cytoplasm. A nucleoius (XI) is present. X 43.000
FIG. 9 (lower). Golgi apparatus of a neurosecretory
cell situated adjacent to the nucleus (X). A few
dense granules (XG) are situated at the periphery
of the Golgi apparatus. The Golgi complex is
composed of membranous lamellae and vesicles of
diffeient si/es (V) containing material of low density. A moderately dense material is present between
the membianous components. X 57,000
PLATE 2
FIG. 3 (above). Ribosome-poor ganglion cell containing two elaborate Golgi complexes (GA). Small
vesicles containing material of light and homogeneous density are located at the ends of the lamellae.
Larger vesicles (V) are scattered throughout the
cytoplasm. Mitochondria (M) are situated at the
ends of the Golgi lamellae where the vesicles appear
to be budding off. The lower Golgi contains an
abundance of small and large membranous vesicles.
A cluster of mitochondria is present in the base
ol a process. Note that the plasma membrane is
irregular, containing numerous crests and indentations. The ganglion cell is completely surrounded
by portions of an epitheliomuscular cell. X 37,000
FIG. 4 (below). Ribosome-rich ganglion cell body
sectioned tangentially through the nucleus (N).
Microtubules extend in a direction parallel to the
long axis of the cell. Xuclear pores (XP) are evident in the nuclear envelope and in some cases aie
approached by miciotubules (arrows). X 29,000
PLATE 3
FIG. 5. Two ribosome-rich ganglion cells. Microtubules (MT) are abundant and extend into the
process (P) of the upper cell. 'The process, in addition, contains riliosomes and mitochondria. Xote
that the upper surface of the process is exposed
to an intercellular space while the lower border
rests on a portion of an epitheliomuscular cell.
GA, Golgi apparatus. X 28,000. Insert. High magnification of area enclosed by box. The nucleus is
surrounded by a double membrane containing pores
(XP). A membranous diaphragm extends across the
pore. Microtubules (MI) and ribosomes are present in the cytoplasm. X54.000
PLA'I E 4
FIG. 6 Supper left). Xuclear region of a ribosomerich ganglion cell illustrating numerous cytoplasmic microtubules cuning inuard towards the nuclear membrane. X 43,000
PLATE 5
FIG. 10 (upper). Xeurosecretory cell containing a
complex Golgi apparatus. Vesicles (V) containing
electron-lucent material and membrane-bounded
dense granules (XG) are situated at the periphery
of the Golgi whose center is occupied by dense
amorphous material. Ribosomes are abundant. 'The
cell is completely enveloped by processes of an
epitheliomuscular cell. X 69,000
FIG. 11 (lower left). Golgi apparatus of a neurosecretory cell. 'Two dense granules are situated in
the dilated ends of the parallel lamellae. X 47,000
FIG. 12 (lower right). Xeurite of a neurosecretory
cell situated at the base of a cnidoblast containing
a nematocyst (Xt). Numerous membrane-bounded
dense granules are present within the process. Some
of the dilated vesicles appear to be empty. X 20,000
PLATE 6
TIC;. 13 Cupper). Process of a neuiosecretory cell
containing dense granules, microtubules (MT), and
ribosomes. Some of the granule-containing vesicles
are situated close to the plasma membiane and
others appear empty. This neurite is situated in
an intercellular space containing small moderately
dense granules. X 62,000
FIG. 14 (lower). Golgi apparatus situated in the
base of a neurite of a neurosecretory cell horn the
base of the animal. Small dense granules appear
within the dilated ends of the parallel lamellae
and as membrane-bounded accumulations adjacent
to the Golgi. Two mitochondria occur in relationship to the Golgi complex. X 124,000
PLATE 7
IK;. 1."). Apc\ ol a sensory cell extending to the
external surface. The plasma membrane is indented
in the region of the sensory cilium (Cj to form an
apical collar (\C). The peripheral fibers of the
modified cilium (G) are sectioned longitudinally,
contain a dense core farrows;, and merge with
348
THOMAS L. LENTZ AND RUSSELL J. BARRNETT
dense material (BB) below the apical collar. From
PLATE 8
this basal bod) (MR) dense 1 outlets (R) splay out
into the cytoplasm. Mitochondria, ribosomes and FIG. 17. Deeply situated neurosensoi) cell contain\csiclcs are present in I lie otoplasm. Mirrnluliiilcs ing nucleus (N): Golgi apparatus (G,\); mitochondria; numerous lice ribosomes and a blunt process
(MT) cMcnd toward the apex. X 57,000
FIG. 16 (insert). Sensory cilium in transverse sec- (!'). A single modified cilium (C) extends in the
tion. There are nine peripheral pairs of fibrils and direction of the external surface. The intercellular
at least four central fibrils. AC, apical collar; N, space surrounding the blunt process is filled with
small dense granules. X 67,000
nucleus. X 60,000
NERVE CELLS IN Hydra
l'LATfc 1
349
350
THOMAS L. LKNTZ AND RTSSKLL }. BARRNF.TT
I'l.A IK 2
NKRVK GKLLS IN Hydra
PLATE 3
351
352
THOMAS L. LENTZ AND RUSSELL J. BARRNETT
PLATE t
NERVE CELLS IN Hydra
PLATE 5
THOMAS L. LENTZ AND RUSSELL J. BARRNETT
PLATE 6
XI-.K\T. Ci I.I.S IN
PLATE 7
Hydra
356
THOMAS L. LENTZ AND RUSSELL J. BARRNETT
PLATE 8