Abdominal Stretch Receptor Organs of Armadillidium vulgare(Crustacea, Isopoda)(Physiology)

5 Pages·1991·1.6 MB·

by  Akiyoshi Nhda

ZOOLOGICAL SCIENCE 8: 187-191 (1991) 1991 Zoological SocietyofJapan
[COMMUNICATION]
Abdominal Stretch Receptor Organs of Armadillidium
vulgare (Crustacea, Isopoda)
Akiyoshi Niida, Kouchi Sadakane
and Tsuneo Yamaguchi
Department of Biology, Faculty of Science, Okayama University,
Okayama 700, Japan
ABSTRACT—The body of the pill bug (Crustacea, receptor organs exert an inhibitory action on the
Isopoda) is composed ofa well-developed thorax and a thoracic stretch receptor organ.
greatlyreducedabdomen. Inspiteofthesmallabdomen,
a pair of stretch receptor organs comprising specialized
muscles and receptorcellsoccuronthe eithersideofthe MATERIALS AND METHODS
midline in the abdomen. All the abdominal stretch
receptor organs show a slowly-adapting response to Experiments were performed on male and
stretch stimuli. The output of an abdominal stretch female pill bugs {Armadillidium vulgare), 12-14
receptor organ blocked impulse discharges from a mm
thoracic stretch receptor organ evoked by an imposed overall length. For morphological identifica-
stimulus, implyingthepresenceofaninhibitoryinterseg- tion of the stretch receptor organs, conventional
mental reflex between them. vital staining with methylene blue and axonal
filling with nickel chloride were employed. In the
latterstainingtechnique, the cut distal stumpfrom
INTRODUCTION
one ofthe four abdominal nerves (Fig. IB), which
Unlike the decapod with a well-developed cara- arise from fused abdominal ganglia, was intro-
M
pace, the body ofthe pill bug, a terrestrial isopod, duced intoaglasscapillary filledwith 0.2 NiCl2.
is predominantly occupied by freely movable Electrical activities ofeach putative stretch recep-
thoracic segments. In this animal we have pre- tor explored in this way were recorded from the
viously shown the occurrence of the thoracic abdominal nerve with the aid of a suction elec-
stretch receptor organs which exclusively show trode.
slowly adapting responses to stretch stimuli [1].
The response characteristic of this sense organ is RESULTS AND DISCUSSION
appropriate to detect sluggish movement of the
thorax accompanying the conglobating behavior As shown in Figure IB, the 8th thoracic gang-
specific to this species. lion is joined by several fused abdominal ganglia
Adjacent to the thorax, there exists the greatly where four abdominal nerves occur on each side.
reduced abdomen, which is composed of six Among these nerves the first contains (see also
abdominal segments. From such a segmental Ab.N. in Fig. 2B) not only the components ofthe
feature, on e would expect remnants of retrograd- 3rd nerve root of the 8th thoracic ganglion, but
ingstretch receptororgansin the abdomen. In this also the axonsofthe stretch receptororgans in the
paper it is reported that the abdominal stretch 1st abdominal segment. To avoid confusion with
the description of the stretch receptor organs, the
Accepted May 21. 199(1 results will be described as from one side only. In
Received March 10. 1990 the 1st to the 5th abdominal segments, identified
188 A. Niida, K. Sadakane and T. Yamaguchi
B
Th.Seg
Ab.Seg.
Th.Seg.8 Ab.Seg.
mm
1
'y{*&^?'
AA A
Fig. 1. (A, B) Schematic illustration of the organization of the thoracic and abdominal stretch receptor organs
viewed from the ventral side, with head and legs removed. The relative size of receptor cells and muscles is
exaggerated. Area enclosed by rectangle in A is shown in B, where the abdomen is depicted as being more
elongated than actual size. Calibration bar in A is not available in B. Ab.G., abdominal ganglion; Ab.N.,
abdominal nerves; Ab.Seg., abdominal segments; ASR, abdominal stretch receptor organ; RC, receptor cell;
RM, receptor muscle; Th.G.8, the 8th thoracic ganglion; Th.Seg, thoracic segment; TSR-l—TSR-4, 1st to 4th
thoracic stretch receptor organs; (C) Photomicrograph of paired stretch receptor organs isolated from the 1st
abdominal segment. This was obtained from a whole-mount preparation stained with methylene blue. The
appearance of the waving receptor muscle (RM) in Figure2C is an artifact which was caused in mounting a
preparationon aslide. Asterisks, obliquelyorientedreceptormuscle;Thickarrowheads, horizontallyarranged
receptor muscle; Thin arrow heads, dendrite from a bipolar receptorcell.
stretch receptor organs are allsimilar in shape and structure andthinsouttowardsposteriorend. The
are much smaller than those in the thorax (Fig. posterior extremities of both components are
1A). Each of the abdominal stretch receptor located on the articular membrane of the anterior
organs comprises a pair of receptor cells and tergal ridge of the subsequent segment. In these
differentiated receptor muscles (Fig. IB, C). The receptor muscles, particular termination of de-
receptor muscles, which lie inparallel andconnect ndrites from two receptor cells can be seen (Fig.
tightly with each other in the anterior part of the 1C); oneextendsalongdendriticprocessalongthe
relevant tergum, run for some distance in the obliquely oriented receptor muscle and this pro-
posterior direction, separating into two muscle cesspresumablyleadstotheposteriorextremityof
components: one is arranged parallel to the thereceptormuscle. Theotherhasashortbulbous
antero-posterioraxisofitsownsegment, whilethe dendrite in the region of the spindle-shaped
otherthickensanddivergesobliquely(Fig. IB, C). structure mentioned above.
The former component forms a spindle-shaped Axons from a pair of receptor cells of the
Stretch Receptor Organ of Pill Bug 189
abdominalstretchreceptororgansruncentrallyvia tion was similar to that illustrated in Figure2B. In
an abdominal nerve. The axonal filling ofthe 2nd this arrangement a preparation was composed of
abdominal stretch receptor organs with nickel the tergal slips of the 1st and 2nd segments
chloride reveals that two axons, oflarge and small containing the 2nd abdominal stretch receptor
caliber, project anteriorly into the brain and organs. The cut distal stump of the abdominal
posteriorly into the fused abdominal ganglion. nerve was introduced into a suction electrode. A
That is. they run medially through the connective vibrator device providing stretch stimulus was
closely parallel to each other. Short secondary driven by a ramp-and-hold pulse. As a result, two
branches of large caliber axon project extensively kind ofimpluse trains, differing in both amplitude
into every thoracic ganglion, while the small and frequency were obtained (Fig. 2A1). These
caliber axon usually lacks secondary branches. impulse trains were usually recorded separately
These modes ofcentral projections ofthe axons of through two window discriminators. The frequen-
the abdominal stretch receptor organs are closely cy plots from impulse trains discriminated in this
similar to that of the thoracic stretch receptor way (Fig. 2A2) showedthateach memberofapair
organs. of abdominal stretch receptor organs is un-
Figure 2A shows electrical activities from the doubtedly ofa slowly adaptingtype, since impulse
2nd abdominal stretch receptor organ. Ex- discharge lasts as long as stretch stimulus is
perimental arrangementforrecordingandstimula- maintained. Thus, it may be inferred that in the
A
Th.G.8 Th.G.7
(D -Ernr Anterior
(2) „100r ?_. 0.5sec
in b
5C »,».,v*».v.
2 8
1
2 4
Time (min) Ab.Seg. Th.Seg.
c
MM nHmMWf*
?!"! i Miff.fei'iiwmiili.aiJi' 1
2 sec
Fig.2. (Al) Responsesofpairedstretch receptororgansfrom the 2nd abdominalsegment. Thestretchstimulusof
the ramp-and-hold form (lower trace, stretch amplitude, 7/^m) elicits two kinds of impulse trains differed in
amplitude: thelargestspikesandslightlysmalleronesoffivepotentialsizes. (A2)Frequencyplotsfromtwokinds
ofimpulse trains evoked by astretch stimulus for a longperiod. Impulse trainswere discriminated throughtwo
windowdiscriminators. Dishcargesofhigh (a)andlow(b)frequenciesduringthequasi-staticphasecontinueata
constant rate for up to 6 min. Stretch amplitude, 7/*m. This was recorded from a separate sample.
(B) Experimental arrangement for showing inhibitory effect ofan abdominal stretch receptor on a neighboring
thoracicstretchreceptororgan. Electricalactivitieswererecordedenpassantwithsuctionelectrodesfromthe 1st
abdominal nerve and the 3rd nerve root in the 7th thoracic ganglion. N. R. 3, 3rd nerve root; V. D., vibration
device. Explanation for other abbreviation: see Fig. 1.
(CI, C2) Records from stretch receptor organs of the 8th thoracic segment and those of the 1st abdominal
segmentinresponsetostretchstimuli,respectively. CI showsinhibitoryeffectsoftheabdominalstretchreceptor
organ on the thoracic stretch receptor organ. In the lower trace ofeach record, upperdeflection represents the
application ofstretch stimulus. Stretch amplitude: 50pm in CI and 3/*m in C2.
190 A. Niida, K. Sadakane and T. Yamaguchi
intact pill bug the tonic impulse discharges from a discharges resulted in the suppression of impulse
pair of abdominal stretch receptor organs change discharges from the 8th thoracic stretch receptor
in proportion to the degree of flexion of the organs.
abdominal segment in a ventral direction. These results indicate the presence ofan inhibi-
Pharmacological application of GABA (>10-5 toryneuron innervatingthereceptorcellofthe 8th
M) tothethoracicstretch receptororganssuppres- thoracic stretch receptor organ. This type of
sed impulsse discharges evoked by an imposed inhibitory effect on the 8th thoracic stretch recep-
stimulus, though the experimental data are not tororgan may be mediatedby an intersegmentally
shown. From available data concerning the located inhibitory neuron which receives inputs
GABA effect on the stretch receptor of the from the ascending axon of the 1st abdominal
A
decapod crustacean [2-4], this suppression indi- stretch receptor neuron. similar inhibitory
cates that GABA is aputative inhibitory transmit- effect has been already reported in the abdominal
ter also in the pill bug, and that GABA inhibitory stretch receptor organs ofthe crayfish [7-9]. Page
synapses [5] may exist on the receptor cells ofthe and Sokolove [9] observed that during voluntary
stretch receptor organs in this animal. On the tonicflexion ofthe abdomen, centrally originating
otherhand, Figure 2Cshowsaninhibitoryeffectof excitatory input to the tonic extensor is removed
the output from an abdonimal stretch receptor and simultaneously high frequency discharge of
organ on a thoracic stretch receptor organ. This AN(accessorynerve)occursinthe2ndnerveroot.
MRO
inhibitory effect was demonstrated on a prepara- This accessory discharge inhibits the tonic
tion as stated below. As shown in Figure2B, (muscle receptororgan) and preventsactivation of
togetherwiththewholenervecode, threeconsecu- MRO-SEMN No. 2 (-superficial extensor moto-
tivetergalslipsweredissectedout: the8ththoracic neuron) reflex, which contributes to the mainte-
tergite containingthoracicstretch receptororgans, nance ofconstantabdominal posture [8]. Thus the
the 1st abdominal tergite with the abdominal MRO-AN reflex is considered to serve as an
stretch receptor organs and the 2nd abdominal intersegmental mechanism to block the MRO-
SEMN
tergite without stretch receptor organs; all the reflex [9].
nerveswere cut away except forthe 1st abdominal It is suggested, therefore that when the animal
nerve and the 3rd nerve root of the 8th thoracic rolls up spherically, an inhibitory intersegmental
ganglion. The preparation made in this way was reflex arisingfrom the abdominal stretch receptors
transferred to a chamber filled with saline for the activates the inhibitory neurons in the more
woodlice [6]. The 1st abdominal tergite was then anterior segement to block the stretch receptor
fixed with insect pins. The rest of free movable organ-superficial extensor motoneuron reflex.
tergites was pulled in a manner as will be briefly
described below. To obtain electrical activities ACKNOWLEDGMENTS
evokedthereby, anen passantextracellularrecord
was made with suction electrodes from the 1st ThisworkwassupportedinpartbyGrantinAidfrom
abdominal nerve and the 3rd nerve root ofthe 7th ttoheTMYinfiosrtrsycioefntEifdiuccaretsieoanr,chS.cience andCulture ofJapan
thoracic ganglion. When the 8th thoracic receptor
muscle was continuously stretched in a constant
REFERENCES
amplitude, a tonic impulse train appeared in the
receptor cells of the 8th thoracic stretch receptor 1 Niida,A.,Sadakane,K. andYamaguchi,T. (1990) J.
organ, as shown in Figure2C, where the impulse exp. Biol., 149: 515-519.
train of another member of a pair of stretch 2 Kuffler, S. W. and Edwards, C. (1958) J. Neurophy-
receptors was eliminated through a window discri- siol., 21: 589-610.
minator. Under this condition, when the 2nd 3 Hori, N., Ikeda, K. and Roberts, E. (1978) Brain
Res., 141: 364-370.
abdominal tergite was pulled by driving the vibra-
4 McGeer, E. G., McGeer, P. L. and McLennan, H.
tion device, there occurred impulse discharges in (1961) J. Neurochem., 8: 36-49.
the 1st abdominal stretch receptor organs. These 5 Elekes, K. and Florey, E. (1987) Neuroscience, 22:
Stretch Receptor Organ of Pill Bug 191
1111-1122. 8 Fields, H. L., Evoy, W. H. and Kennedy, D. (1967)
Holley. A. and Delaleu. J. C. (1972) J. exp. Biol., J- Neurophysiol., 30: 859-875.
57:589-608. 9 Page,C. H. andSokolove,P. G. (1972) Science, 175:
Eckert. R. O. (1961) J.cell.comp. Physiol.,57: 149- 647-650.
162.