Peripheral innervation patterns and central distribution of fin chromatophore motoneurons in the cuttlefish Sepia officinalis
Institute of Neuroscience, 1254 University of Oregon, Eugene, OR 97403-1254, USA
* Author for correspondence (e-mail: gaston{at}uoneuro.uoregon.edu)
Accepted 17 June 2004
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Summary |
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Key words: body patterning behavior, cephalopod, cuttlefish, Sepia officinalis, chromatophore, fin nerve, chromatophore motoneuron
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Introduction |
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Body patterning behavior in cephalopods is generated by various
combinations of postural, textural and chromatic elements. The chromatic
elements dominate, however, with thousands to millions of chromatophore organs
[referred to hereafter as `chromatophore(s)' for convenience] located
throughout the dermis of each animal
(Hanlon and Messenger, 1988).
Each chromatophore is a pigment-containing organ (yellow, orange, or dark
brown; Hanlon and Messenger,
1988
) with radially emanating muscle fibers that are under direct
neuromuscular control (Florey,
1966
; Cloney and Florey,
1968
). This direct innervation allows complex patterns to be
created and changed rapidly (in less than a second), making cephalopod
chromatophores and their resultant detailed patterns unique within the animal
kingdom.
Chromatophore physiology has been investigated in a variety of studies in
the past half century (for a review, see
Messenger, 2001). To broaden
the scope of understanding of cephalopod body patterning behavior, this study
focuses on the motoneurons that control chromatophores. Little information
exists concerning this level of chromatophore control, particularly in the
cuttlefish, whose remarkable repertoire of color patterns perhaps best
illustrates the complexities of cephalopod body patterning
(Hanlon and Messenger, 1988
).
Previous nerve degeneration, stimulation and retrograde labeling studies in
various species of cephalopods suggest that chromatophore motoneuron somata
reside in the chromatophore lobes of the brain
(Sereni and Young, 1932
;
Boycott, 1961
; Dubas et al.,
1986a
,b
);
however, subsets of chromatophore motoneuron somata that control specific
motor fields have yet to be identified and localized in any cephalopod.
This paper takes a step toward localizing and identifying individual
chromatophore motoneurons that control chromatophore motor fields of the fin
in the European cuttlefish Sepia officinalis. Motoneurons innervating
the fin, as shown in squid (Dubas et al.,
1986a,b
),
likely originate in the posterior subesophageal mass (PSEM) of the brain. In
Sepia, the PSEM consists of five paired lobes: the posterior
chromatophore lobe (PCL), the posterior posterior chromatophore lobe
(PPCL), the fin lobe (FL), the palliovisceral lobe (PVL), and the
magnocellular lobe (MCL) (Boycott,
1961
; Loi and Tublitz,
2000
). Although squid and cuttlefish have many similarities, their
body patterns differ greatly in complexity, and thus it is possible that the
location of chromatophore motoneurons may differ as well. This difference in
location may be especially true for fin chromatophores, as a squid's fin is
located only at the posterior end of the mantle while a cuttlefish fin extends
the entire length of the mantle.
Fin chromatophores and their associated motoneurons are of specific
interest due to previous work on the fin of the cuttlefish
(Loi et al., 1996; Loi and
Tublitz, 1997
,
2000
). The translucent fin is
well suited for chromatophore studies, as chromatophore activity is highly
visible in this region, and compared to other parts of the body, there are
relatively fewer non-chromatophore muscles in the fin, which somewhat
simplifies analysis. Chromatophores of the fin are innervated by the fin
nerve, a large nerve that leaves the pallial nerve on each side of the body
medial to the stellate ganglion and runs dorsally through a foramen in the
mantle wall (Hillig, 1912
;
Tompsett, 1939
). This nerve,
in addition to containing axons innervating chromatophore muscles, also
contains afferent fibers as well as axons innervating fin muscles
(Kier et al., 1985
). Once
removing overlying mantle skin and muscle, the fin nerve is easily
identifiable with its multiple branches spreading over the dorsal mantle wall
(see Fig. 1). Hillig
(1912
) reported 25-30 fin
nerve branches in Sepia and briefly described these branches as
falling into posterior, middle and anterior groups. These three categories are
not definitively named or outlined, however. Also, the number of branches
reported is a range at or near the point where the branches enter the fin;
more proximal branch counts are not mentioned.
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In this paper, the fin nerve and its branching pattern are further characterized, and a naming system for fin nerve branches is presented to aid in the location of branches across individuals. Through extracellular stimulation of fin nerve branches, chromatophore motor fields of individual nerves were mapped as well. To determine the origin of motoneuron axons in the fin nerve and thus the central location of fin chromatophore motoneurons, individual fin nerve branches were retrogradedly labeled with dye. Data presented here reveal a topographic arrangement of the nerve branches innervating the fin. In addition, retrograde labeling data identify the PSEM as the primary location of fin chromatophore motoneurons.
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Materials and methods |
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Fin nerve stimulations
Fin nerve stimulations were performed on intact male and female young
adult/adult animals with mantle lengths ranging from 9-20 cm. Following
anesthetization with 1% ethanol in ASW, cuttlefish were partially
immobilized by being pinned in a Sylgard-lined container with continuously
flowing oxygenated ASW (room temperature, 23-25°C). Ethanol was added as
needed to keep the animal lightly anesthetized during experimentation.
The fin nerve was exposed by dissecting away overlying skin and muscle
layers. Suction electrodes of varying tip diameters (0.5-1.5 mm) filled with
ASW were used to seal onto individual fin nerve branches one at a time.
Stimulations were performed with a Grass stimulator (Model S4K); the
parameters for square-wave DC pulses were as follows: frequency, 1 Hz; delay,
1 s; duration, 10 ms; voltage, 0.5-5.0 V. Elicited chromatophore activity was
documented immediately following each stimulation through hand drawings from
visual observations. Reflecting elements (leucophores;
Packard and Sanders, 1971;
Messenger, 1974
) in the fin
and mantle skin served as reliable landmarks when establishing the region of
chromatophore activity. Regions of electrically evoked activity were measured
as the straight line distances along the fin where chromatophore activity was
present. Videotapes of experiments were used to confirm and refine the data
collected during each stimulation experiment.
Retrograde dye labeling
Juvenile animals with mantle lengths ranging from 4-8 cm were used in all
backfill studies. Following anesthetization and partial immobilization of the
animal as described above, the fin nerve was exposed on one side of the body
by dissecting away a minimal amount of overlying skin and muscle layers. 1-2
µl of 5% Texas Red dextran (10 000 MW; Molecular Probes, Eugene, OR, USA)
in 0.20 µm filter-sterilized ASW were injected into the desired fin nerve
branch using a 10 µl Hamilton (Reno, NV, USA) syringe. To facilitate
penetration of the nerve, a sharp microelectrode tip was sealed onto the end
of the syringe. Following a single unilateral dye injection, each animal was
returned to a tank of ASW for 25-63 days (depending on animal size), the first
day of which was in darkness. After allowing sufficient time for the dye to
travel, the brain (with surrounding tissue and cartilage) was removed and
fixed overnight in 4% paraformaldehyde. Leaving the cartilage intact, the
fixed brain was trimmed of surrounding tissue and saturated with 20% sucrose
for cryosectioning. Although the contralateral side of the brain of injected
animals served as a control, the brain of one uninjected animal was processed
in the same manner described above and served as another control.
Observation of labeled cells
Each brain from retrograde labeling experiments was sagittally
cryosectioned at 30 µm from the appearance of the posterior subesophageal
mass on one side of the brain to its disappearance on the opposite side.
Sections were adhered to precleaned slides (Superfrost/Plus; Fisher,
Pittsburgh, PA, USA) and then dehydrated (3 min each in 30, 50, 70, 90, 95 and
100% ethanol), cleared in xylene (5 min), and mounted in Permount (Fisher,
Pittsburgh, PA, USA). UV fluorescence microscopes with Texas Red or TRITC
filters were used to visualize labeled cells. To accentuate the visibility of
true labeling and reduce the visibility of autofluorescence, cell counts were
performed under a triple filter (DAPI/FITC/Texas Red). Images were acquired
with a Zeiss 310 confocal microscope, as well as with a Nikon Coolpix 990
digital camera.
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Results |
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Fig. 1 depicts a drawing of
a bilateral fin nerve branching pattern from one animal
(Fig. 1A) and a photograph of
fin nerve branches and interspersed blood vessels from a different animal
(Fig. 1B). At the most broadly
conserved level between animals, two main groups of branches exist: anterior
and posterior (red and purple, respectively, in the upper part of
Fig. 1A, and `a' and `p' in
Fig. 1B). The anterior group
consists of 3-6 primary (1°) branches, while the posterior group contains
3-5 1° branches. Before entering the fin, these 1° nerves almost
always further branch into secondary (2°), tertiary (3°), and
quaternary (4°) nerves (orange, yellow, green, and blue nerves in the
lower half of Fig. 1A).
Although a third `middle' group has previously been proposed by Hillig
(1912), this group has here
been combined with the anterior group, as the point at which the fin nerve
emerges through the mantle wall differentiates into only two groups, those
leading anteriorly and those leading posteriorly. This two-group
classification simplifies an already complex map of fin nerve branches and
their associated chromatophore motor fields.
To aid in locating individual branch position across animals, a naming system for fin nerve branches was devised (Fig. 1A). The name of each branch begins with a capital letter, A or P, signifying anterior or posterior, respectively. Numbers and lower-case letters are then added alternately to designate the various levels of branching (i.e., 1°=A/P + number, 2°=A/P + number + letter, 3°=A/P + number + letter + number, etc.). As an illustration, the orange colored nerve in Fig. 1A is labeled A1, as it is the first 1° anterior branch. This nerve separates into two 2° branches, A1a and A1b; four 3° branches, A1a1, A1a2, A1b1, A1b2; and two 4° branches, A1a2a and A1a2b. Anterior branches are labeled consecutively from anterior to posterior, while posterior branches are labeled consecutively from posterior to anterior. As not all animals have the same number of fin nerve branches or the same branching pattern, branches with the same name in different animals may not activate identical motor fields. Thus, this naming system serves only as a reference for the location of individual branches and not as a means to compare chromatophore motor fields across individual animals.
Fin nerve branching in Sepia is not invariant across or within individuals, and an analysis of the percentage of preparations (N=22) having different numbers of branches at each of four levels of branching revealed interesting differences. First, by observing variability in the occurrence of branches at a particular level (i.e., 1°, 2°, etc.), it was noted that all preparations showed 1° and 2° branching in both anterior and posterior fin nerves, most exhibited 3° branching (91% for both anterior and posterior), and some manifested 4° branching (45% anterior, 18% posterior). Second, variability in the number of branches at each of the various levels was present as well. This variability increased beyond the 1° level of branching in both anterior and posterior branches and was highest for 2° and 3° branches, as seen by the range of the number of branches present at each level (1°, 3-6 anterior and 3-5 posterior branches; 2°, 2-12 anterior and 4-8 posterior branches; 3°, 0-10 anterior and 0-12 posterior branches; 4°, 0-6 anterior and 0-4 posterior branches). Lastly, the number of branches at each level that branch to form the next level also varied. An analysis of this aspect of variability showed that primary branches most often branched to the next highest level, yielding 2° branches 78% and 69% of the time for anterior and posterior branches, respectively. In addition, secondary branches yielded 3° branches 27% (anterior) and 30% (posterior) of the time, while 3° branches yielded 4° branches 16% (anterior) and 6% (posterior) of the time.
Despite the variable nature of fin nerve branching described above, individual fin nerve branches remain identifiable from one preparation to the next. Although the variability creates difficulty in recognizing identical branches between individuals, it does not detract from identifying branches located in similar positions across animals. The ability to recognize such branches in similar locales allows for comparative studies on the fin nerves and the chromatophores they innervate.
Stimulation of fin nerve branches
Extracellular stimulation of individual fin nerve branches (N=99
branches from 15 animals) caused groups of chromatophores to expand
(Fig. 2) and elicited fin
movement as well. Anterior branches activated anterior clusters of fin
chromatophores, while posterior branches activated more posterior clusters
(Figs 2,
3). This topographic
innervation was observed in both 1°
(Fig. 3A) and 2° branches
(Fig. 3B). Often there was some
overlap between the areas neighboring branches activated, especially between
2° branches.
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All three color classes of chromatophores (yellow, orange, dark brown) were activated during the above stimulations, and expansion occurred at the same frequency as the stimulus. All chromatophores that expanded during stimulation retracted upon cessation of the stimulus, although at times yellow chromatophores appeared to have a slower retraction rate. On several occasions, some chromatophores were expanded throughout the experiment; other times, spontaneous chromatophore activity was present.
In addition to chromatophore activity, fin movement frequently occurred during stimulations. In 89% of all nerves stimulated (88 of 99 stimulated nerves), chromatophores and fin skeletal muscles were activated simultaneously, while chromatophore activity occurred alone in the remaining 11%. Fin movement was not observed in the absence of chromatophore activity. Although the voltage required to elicit fin movement varied, fin movement always occurred at an equivalent or higher threshold voltage than that required to elicit chromatophore activity.
Chromatophore activity (i.e. number of chromatophores activated) on the fin increased in a voltage-dependent manner. At a certain voltage level, the entire motor field became active. Beyond this voltage level, there appeared to be no further increase in chromatophore recruitment; instead, an increase in the apparent size of individual chromatophores was often observed. Thus, motor fields were mapped at the minimum voltage (most typically about 2 V) that elicited full activation of a branch's entire motor field.
Retrograde labeling of fin nerve branches
Retrograde labeling of individual fin nerve branches (N=3 branches
from three animals; Fig. 4A)
revealed the posterior subesophageal mass (PSEM) of the Sepia brain
to be the primary location of labeled motoneurons
(Fig. 4B). This region of the
brain consists of a central neuropil surrounded by a multi-layered rind of
cell bodies. Secondary locations of labeled cells in the Sepia
nervous system consisted of the brachial lobe (BRL;
Fig. 4B) in the anterior
subesophageal mass (ASEM) and the stellate ganglion (SG;
Fig. 4C) in the periphery.
Labeled motoneurons were presumed to be primarily chromatophore and fin muscle
motoneurons since stimulation of fin nerve branches caused both chromatophore
expansion and fin movement (see above results). All labeled cells were
ipsilateral to the dye-filled nerve, and both contralateral and uninjected
controls contained no labeled cells. The uninjected control was necessary
since both ipsilateral and contralateral neurons could have been labeled in
injected animals.
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Within the PSEM of the Sepia brain, labeled motoneurons were found
in four of the five lobes that compose the mass. Three of these lobes were the
posterior chromatophore lobe (PCL), the fin lobe (FL), and the palliovisceral
lobe (PVL) (Fig. 5A,B). The
fourth lobe, a smaller lobe described by Loi and Tublitz
(2000) and termed the
posterior posterior chromatophore lobe (PPCL), contained a few
labeled cells (photo not shown). The fifth lobe, the magnocellular lobe (MCL),
contained no labeled cells. Most labeled cells were located more laterally
than medially in the PSEM. Additionally, they ranged in size from about 20-80
µm (Fig. 5C,D), with somata
in the PCL, PPCL, and PVL typically smaller than those in the FL.
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The total number of cells labeled in each of the three retrograde labeling experiments presented here (branches A1, P1 and A1a) is shown in Fig. 6A. Both 1° nerve dye fills yielded a similar number of labeled cells (742 for A1, 734 for P1), while the smaller 2° nerve A1a had fewer labeled cells (476). For both anterior nerves (A1 and A1a), these cell counts represent all cells labeled in the PSEM, BRL and SG. The same is true for the posterior nerve (P1), with the exception that the SG was not included because it was not sectioned. It is unlikely that the omission of the SG in this case would cause a significant increase in the number of cells labeled in the posterior nerve fill, as there were only two cells labeled in the SG of each anterior nerve fill (see below). Since nerves A1 and P1 are of an equivalent branch level and since they had similar numbers of cells labeled in each brain lobe (see below), the similarity is predicted to extend to the SG as well.
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Of the total number of cells labeled, most were located in the PSEM (Fig. 6B). For each nerve, the percentage of labeled cells in the PSEM was >97%, with the remaining cells falling outside of the PSEM in the BRL and SG. In the case of branch P1, cells outside of the PSEM are only those cells that were labeled in the BRL since the SG was not sectioned.
The distribution of labeled cells is further depicted in Fig. 7, where the percentage of cells in each brain lobe and in the SG is shown. As can be seen, the majority of labeled cells lie in the PSEM. Within the PSEM, cells are primarily in the PCL and FL and secondarily in the PVL, with no labeled cells located in the MCL. The percentage of cells in the PPCL, as well as in both the BRL and the SG, is minimal as compared to other regions of the PSEM.
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Discussion |
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Topographic organization of the fin nerve
Extracellular stimulation of chromatophore nerves has previously been
conducted in Sepia (Maynard,
1967) as well as in other cephalopods
(Florey, 1966
;
Florey and Kriebel, 1969
;
Dubas and Boyle, 1985
;
Dubas, 1987
). In those studies,
single or small bundles of axons were stimulated to examine innervation at
either the single chromatophore muscle or the single motor unit levels. Other
studies in octopus (Rowell,
1963
; Sanders and Young,
1974
; Bühler et al.,
1975
) and squid (Ferguson et
al., 1988
) have examined effects of stimulating larger
chromatophore nerve bundles. The present study reports observations made by
stimulating large bundles of axons composing entire branches of the
Sepia fin nerve, revealing a topographic innervation pattern of fin
chromatophores in which anterior branches activated anterior clusters of fin
chromatophores and posterior branches activated more posterior clusters.
Topographic representation of peripheral elements by the nervous system
appears to be a recurring feature in cephalopods. Saidel has shown topography
in Octopus with respect to the relationship between photoreceptor
terminals and centrifugal cell bodies in the optic lobes
(Saidel, 1979) as well as
between the optic and peduncle lobes
(Saidel, 1981
). Also in
Octopus, Monsell
(1980
) reported such an
arrangement between motoneurons in the stellate ganglia and the mantle muscles
that they innervate. In squid, Ferguson et al.
(1988
) demonstrated a
topographical arrangement of peripheral stellar nerves by mapping their motor
fields. Additionally, sensory receptive field mapping via mechanical
stimulation of the fin in Sepia
(Kier et al., 1985
) revealed a
topographic arrangement of the fin nerves. The present study extends these
findings to the chromatophore system and is the first to report topography by
peripheral fin nerves innervating the chromatophore system.
Location of fin chromatophore motoneurons
Several previous studies in cephalopods have contributed data concerning
the location of chromatophore motoneurons. For example, Sereni and Young
(1932) conducted nerve
degeneration studies in various cephalopods, concluding that chromatophore
motoneuron axons pass through the SG without synapse and originate in the
brain. Decades later, chromatophore motoneurons were further localized to
subesophageal centers of the brain by Boycott
(1961
); his extracellular brain
stimulations showed that stimulation of the anterior chromatophore lobe (ACL)
and the PCL elicited chromatophore activity in anterior and posterior regions
of Sepia, respectively. Years later, retrograde labeling studies in
the squid Lolliguncula also showed chromatophore motoneurons to be
located in subesophageal centers of the brain (Dubas et al.,
1986a
,b
).
However, these authors showed that posterior chromatophores had motoneurons
located not only in the PCL but also in other lobes of the PSEM (i.e. FL, PVL,
MCL). As these retrograde labeling experiments in squid were performed by
pushing solid crystals of horseradish peroxidase (HRP) under the skin, it is
likely that other types of motoneurons were labeled, such as skin, fin and
mantle muscle motoneurons. In addition, it is possible that HRP crossed gap
junctions and consequently labeled cells upstream of the chromatophore
motoneurons. Thus, it is unclear if motoneurons controlling chromatophores in
posterior body regions reside only in the PCL
(Boycott, 1961
), are scattered
across various lobes of the PSEM (Dubas et al.,
1986a
,b
),
or are in different locations in cuttlefish and squid. In the present study, a
solubilized dye was injected directly into fin nerve branches. Although this
injection method may have failed to label a small percentage of axons within a
fin nerve branch, it minimized labeling of other types of motoneurons, thus
revealing the primary location of chromatophore motoneurons of fin
chromatophores in Sepia to be the lobes of the PSEM.
Although labeling of other types of motoneurons (i.e. skin and mantle muscle motoneurons) was minimized by the direct, highly localized nerve injections described here, it is probable that at least one other type of motoneuron was labeled: fin muscle motoneurons. Like chromatophore motoneuron axons, fin muscle motoneuron axons innervate the fin through the fin nerve branches, as revealed by stimulation experiments reported in the present study. As the axonal composition of fin nerve branches was not examined, the proportion of each type of axon present in fin nerve branches remains to be determined. In addition, differentiation between the two types of labeled motoneurons in the PSEM remains to be explored as well. Preliminary experiments in Sepia indicate that fin chromatophore motoneurons are likely distributed across at least the PCL and FL (M. R. Gaston and N. J. Tublitz, unpublished observation).
Although most labeled neuronal somata were found in the lobes of the PSEM,
1-2% of labeled cells from each nerve fill were located in other regions of
the Sepia nervous system. These areas were the BRL in the anterior
subesophageal mass of the brain and the SG in the periphery. There are several
probable explanations for the labeling of these few outlying somata. One
explanation is that a small amount of dye may have leaked from the injected
nerve, with subsequent transport by axons in the surrounding tissue. Since fin
nerve branches come into close contact with mantle muscle, this explanation
most likely explains the very small number of SG labeled cells, as the SG is
the site of at least some mantle muscle motoneuron somata
(Sereni and Young, 1932;
Young, 1971
,
1976
; Dubas et al.,
1986a
,b
).
As for the BRL, Boycott
(1961) reported that
extracellular stimulation of this region proper in Sepia caused arm
movements not typically observed in the animal's life and did not cause
chromatophore expansion on the head or arms. According to P. K. Loi (personal
communication), some cells in the anterior region of the subesophageal mass
(i.e. the BRL) express FMRFamide-like immunoreactivity. Since previous work in
Sepia has shown the FMRFamide family of neuropeptides to act as
excitatory transmitters at the chromatophore neuromuscular junction
(Loi et al., 1996
;
Loi and Tublitz, 2000
), it is
possible that labeled cells in the BRL could be chromatophore motoneurons.
Having anteriorly located chromatophore motoneurons that innervate
chromatophores in posterior regions of the body could be advantageous in a
cephalopod for coordination of body patterning between anterior and posterior
parts of the animal. This type of coordination would be critical, for example,
for successful avoidance of detection (by predators and/or prey) through
camouflage. Of all cephalopods, Sepia seems the most likely candidate
to possess such a coordination system since it is thought to produce the most
complex body patterns in its taxonomic class.
Organization of fin chromatophore motoneurons
The results presented here lead to the obvious question of whether
chromatophore motoneuron somata in the brain are arranged somatotopically.
Boycott (1961) demonstrated
that extracellular stimulation of the ACL and PCL in the Sepia brain
activated anterior and posterior regions of the body, respectively. He further
described somatotopy within the PCL by demonstrating that stimulation of
anterior or posterior regions of this lobe activated anterior or posterior
regions of mantle chromatophores, respectively. In the squid
Lolliguncula, brain stimulation and retrograde labeling studies by
Dubas et al.
(1986a
,b
)
suggest that no somatotopic arrangement exists within the PCL. Although these
studies draw different conclusions, they may reflect a species-specific
difference in brain organization between cuttlefish and squid, since body
patterning complexity differs markedly between the two species. Most squid are
open-water animals that have a relatively small number of chromatophores;
their patterns are simplistic, as the animals are faced with concealing
themselves in the `transparent' water column
(Hanlon and Messenger, 1988
).
Cuttlefish, however, possess significantly greater numbers of chromatophores
than seen in squid (200-500 chromatophores mm-2 for Sepia
officinalis (Hanlon and Messenger,
1988
) versus 8 chromatophores mm-2 for
Loligo plei (Hanlon,
1982
; Hanlon and Messenger,
1988
)). The increased density of chromatophores in cuttlefish is
used to produce the much more intricate patterns necessary for successful
concealment in their preferred habitat, the substrate of coastal waters
(Hanlon and Messenger, 1988
).
It is this more complex patterning by the cuttlefish that may necessitate a
more systematic arrangement of somata in the brain as well as axons in the
periphery. Future experiments in Sepia should extend the findings of
Boycott (1961
) and perhaps
extend the results of the present study to include other peripheral nerves
such as those leading to the mantle and arms. Although not addressed in this
study, there is much to be learned from the finer details of peripheral
chromatophore innervation, especially how the chromatophores act in concert
with reflecting elements in the skin to produce body patterns. The goal,
however, is to determine if the location of individual motoneuron somata in
the brain of the cuttlefish mirrors peripheral topographic patterns of
organization. Identification of the arrangement of motoneuron somata will
facilitate future experiments aimed at elucidating the mechanisms underlying
chromatophore control and, in turn, cephalopod body patterning behavior.
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Acknowledgments |
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References |
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