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Functional organisation of anterior thoracic stretch receptors in the deep-sea isopod Bathynomus doederleini: behavioural, morphological and physiological studies

Masazumi Iwasaki¹, Ayako Ohata¹, Yoshinori Okada¹, Hideo Sekiguchi² and Akiyoshi Niida^1,*

¹ Department of Biology, Faculty of Science, Okayama University, Tsushima, Okayama 700-8530, Japan and
² Faculty of Bioresources, Mie University, Japan

View larger version (20K): [in a new window]   Fig. 1. Experimental arrangement for recording digging behaviour (A) and the method used to measure segmental deflection (B). (A) L-shaped acrylic walls were placed in an aquarium to induce digging behaviour. Solid gelatine served as a substratum. The sea water was aerated and kept at 14°C. (B) Points a and b indicate the anterior and posterior margins of the head, respectively. Similarly, points c and d indicate the posterior margins of the second and third thoracic segments, respectively. For the second thoracic segment, lines ab and bc formed the angles of extension and flexion. For a more detailed explanation, see the text.

View larger version (32K): [in a new window]   Fig. 2. Procedure (A) for recording stretch-activated responses of TSR-1 and (B) for demonstrating intersegmental inhibition of TSR-2 by TSR-3. All the ganglia except the first (A) and the second and the third (B) thoracic ganglia were cut off. TSR-1 was activated by moving the head in a horizontal direction with forceps mounted on a small micromanipulator connected to a vibration device. Stretch-activated responses of TSRs were recorded en passant from N3. N3, nerve 3; TG1, first thoracic ganglion; TS2, second thoracic segment; TSRs, thoracic stretch receptors; VD, vibration device; SM, small micromanipulator.

View larger version (47K): [in a new window]   Fig. 3. Digging behaviour of Bathynomus doederleini. Video frames show (A) the start of digging of a burrow, (B) advancing towards the bottom, using the thoracic legs and beating swimmerets, (C) reversing direction by rolling up to leave the burrow and (D) creeping out of the burrow. This animal was 11 cm long.

View larger version (22K): [in a new window]   Fig. 4. (A) Flexion and extension of the thoracic and abdominal segments during digging. Measurements were based on 6–8 selected video frames per animal (N=8). The drawings show extension and flexion of body segments. (B) The maximum angles of body segments during roll-up. The position of the animal during rolling up is shown in the drawing. Measurements were made as in A. Each column in A and B represents the mean value ± S.E.M. AS, abdominal segment; TS, thoracic segment. Numerals indicate numbers of body segments.

View larger version (46K): [in a new window]   Fig. 5. (A) Lateral view of the spatial organisation of thoracic and abdominal stretch receptors. Segmental stretch receptors are located on the dorsal side and extend axons that run towards the central nervous system (CNS) via nerve 3 (N3). Note that, as in crayfish, the axons of the abdominal stretch receptors project to the eighth thoracic ganglion. (B) The CNS and central projection of the axon of TSR-2. The CNS is depicted dorsally, and the CNS posterior to TG3 is not drawn, and the oesophageal connectives are interrupted. Ascending and descending central projections of the axon of TSR-2 are shown (camera lucida drawing). This was revealed by electrophoretically applying Lucifer Yellow to the centrifugal cut end of N3. (C) Ventral view of the organisation of thoracic stretch receptors. Thoracic stretch receptors are located dorsally and bilaterally. Dendritic branches from the receptor cell of TSR-1 innervate the extensor muscle, while those of TSR-2 entwine with the receptor muscle-like strand, which is exaggerated in size. TSR-3 to TSR-7 have two receptor cells and a single receptor muscle. AS, abdominal segment; ASR, abdominal stretch receptor; TS, thoracic segment; TSR, thoracic stretch receptor; ROS, rostrum; Deutero, deuterocerebrum; Mx, maxillary nerve; Proto, protocerebrum; Trito, tritocerebrum; TG, thoracic ganglion.

View larger version (109K): [in a new window]   Fig. 6. TSR-1 revealed by the application of Lucifer Yellow to the peripheral cut end of the dorsal nerve. Dendritic branches from the anterior pole of a fusiform receptor cell fan out on the extensor muscle, and a motor nerve (MN) runs antero-medially from the posterior pole. The inset shows the area around the motor nerve indicated by the arrow, demonstrating that fine branches extend out from the large MN. The MN was broken artificially. RC, receptor cell. Scale bar, 200 µm.

View larger version (132K): [in a new window]   Fig. 7. Three examples of TSR-2s filled with Lucifer Yellow. (A) This example was photographed simultaneously under normal and ultraviolet light. Two dendritic branches from the fusiform receptor cell run anteriorly in contact with the receptor muscle-like strand (dotted lines), and their fine dendritic branches terminate in the neighbouring extensor muscle fibre (small arrows within the rectangle). (B) Two anterior dendrites from a fusiform receptor cell entwine with the muscle strand (asterisks), and a fine dendritic branch on the medial side terminates in the juxtaposed extensor muscle fibre (arrow in the area enclosed by a rectangle and shown in the inset). (C) Fluorescent photomicrograph. The fusiform receptor cell gives off an anteriorly directed stem dendrite, from which a small dendrite entwines with the muscle strand (asterisks) and two dendritic branches bifurcate; one runs towards the neighbouring extensor muscle (arrows) and the other entwines with the muscle strand. In this example, an axon from the posterior pole of the receptor cell can be clearly seen. An, anterior; EMF, extensor muscle fibre; L, lateral; M, medial; P, posterior. Directions in A apply to B and C. All scale bars, 400 µm.

View larger version (52K): [in a new window]   Fig. 8. A NiCl2 fill of TSR-3, which consists of a single receptor muscle (RM) and triangular (RC1) and fusiform (RC2) receptor cells. White arrows indicate dendrites of RC1, which extend along the entire receptor muscle in a V-shaped manner. The black arrow shows the stout dendrite of RC2, which terminates in the central part of the receptor muscle. Since the receptor muscle is long, it is cut off at both sides. This photograph was made under a polarised light microscope. The receptor muscle shows birefringence. Scale bar, 400 µm.

View larger version (33K): [in a new window]   Fig. 9. Response characteristics of TSR-1 and TSR-2 to stretch stimuli. Both TSR-1 (A) and TSR-2 (B) (see insets) show slowly adapting impulse discharges in response to a stretch stimulus (time scales: 3 s in A and 5 s in B) but, as seen from the impulse frequency/stretch amplitude relationship, TSR-2 has a wider dynamic range than TSR-1. The impulse frequency/stretch relationship of TSR-2 is linear between 0.2 and 3.8 mm. The two examples in A and B were obtained from separate animals. The plots were obtained by counting impulses during the static phase within 5 s of initiation of a stretch stimulus.

View larger version (36K): [in a new window]   Fig. 10. Stretch-activated response of TSR-3 and TSR-4. (Ai) Two kinds of slowly adapting impulse discharges in TSR-3 (amplitude of stretch stimulus 1.2 mm). These responses were further analysed through two sets of window discriminators to show phasico-tonic (Aii) and tonic (Aiii) responses. (Bi) The stretch-activated response of TSR-4 has two kinds of slowly adapting impulse discharge: phasico-tonic (Bii) and tonic (Biii) responses (amplitude of stretch stimulus 1.5 mm). These responses were separated through the window discriminator and are illustrated as frequency histograms. Note that TSR-3 and TSR-4 responses last as long as a stretch stimulus is applied. In this case, both responses continue for approximately 3 min.

View larger version (37K): [in a new window]   Fig. 11. Responsiveness of TSR-3 and TSR-4 to the same amplitude of stretching. (A) The inset shows stretch-activated responses of TSR-3, which consist of a phasico-tonic response (i) and a tonic response (ii). Scale bar, 10 s. The impulse frequency/stretch relationships for the phasico-tonic and tonic responses are shown separately in A and B. Both the phasico-tonic and tonic stretch receptors respond to a stretch of up to 3.8 mm without saturation. (C,D) The inset shows stretch-activated responses of TSR-4. Scale bar, 10 s. The impulse frequency/stretch relationship is presented in the same manner as for TSR-3. Both phasico-tonic (ii) and tonic (iv) responses at a stretch of 3.8 mm appear to reach a plateau impulse frequency or show a decrease in impulse frequency. The same signals indicate a pair of phasico-tonic and tonic responses from one animal.

View larger version (17K): [in a new window]   Fig. 12. Responses of TSR-2 in situ to flexion of the thorax. Experiments were performed on two animals. The inset shows that the anterior thoracic tergite was moved manually in the direction of the double-headed arrow. is the flexion angle of the second thoracic tergite, which was varied manually by means of a micromanipulator. Flexion-induced activity was recorded en passant from nerve 3 of the second thoracic ganglion. The anterior and posterior connectives to the second thoracic ganglion were cut.

View larger version (18K): [in a new window]   Fig. 13. Intersegmental inhibitory effect of TSR-3 on TSR-2. Stretch-induced discharges of TSR-2 are interrupted (A) by stretch-induced activity of TSR-3 (C). The upward deflection of the lower trace in C shows three consecutive stretch stimuli of 1.0 mm. These interruptions are also displayed through a window discriminator (B). The application of a stretch stimulus (1.2 mm) to TSR-2 is indicated by an upward deflection in the trace below B. (D) The region of the recording indicated by double-headed arrows in A shown on an expanded time scale. In nerve 3, small spikes (spike height indicated by facing double arrows to the right of the trace) correspond to the appearance of stretch-activated responses of TSR-3, whose responses are also presented as a frequency histogram.

View larger version (41K): [in a new window]   Fig. 14. Intersegmental inhibitory effect of TSR-4 on TSR-3. The receptor muscle of TSR-3 was stretched manually (upward deflection below trace C), resulting in phasico-tonic (large spikes) and tonic (middle-sized spikes) impulse discharges (A). These responses are also shown in B and C through two sets of window discriminators. Since the stretch stimulus was delivered slowly, unevenness was seen in the rising phase of a stretch stimulus. After reaching a given stretch length, the receptor muscle of TSR-4 was stretched repeatedly (F). The stretch amplitudes were given in the order 0.7, 0.7, 1.0 and 1.0 mm. The impulse discharges of TSR-3 are suppressed at a stretch length of 1 mm in TSR-4 (B), but this inhibitory effect was weaker for tonic responses (C). Impulse discharges of the putative accessory neurone through a window discriminator (D) and its frequency histogram (E). (G) The region indicated by double-headed arrows in A shown on an expanded scale. Small spikes in nerve 3 (spike height indicated by facing double arrows to the right of the trace) coincide with the appearance of stretch-activated responses of TSR-4, whose small spikes are also presented as a frequency histogram (E).

View larger version (29K): [in a new window]   Fig. 15. Effect of bath-applied GABA on TSR-2. Inhibitory effects of GABA were observed at three different concentrations. In each experiment, GABA was applied to the same preparation after allowing it to recover from the previous dose of GABA by washing thoroughly (3 min) with normal saline. Bars indicate superfusion with GABA.