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First published online October 10, 2003

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Sensory innervation of the ovotestis in the snail Helix aspersa

Tomasz Antkowiak and Ronald Chase^*

Department of Biology, McGill University, 1205 Ave Docteur Penfield, Montreal, Quebec, H3A 1B1, Canada

View larger version (37K): [in a new window]   Fig. 1. Schematic drawing of the semi-intact preparation and perfusion dish. During some experiments, the gap in the centre of the dish was perfused with sucrose to reduce efferent traffic in the intestinal nerve; otherwise, all tissues were bathed in saline. AG, albumen gland; CNS, central nervous system; D, distal; DG, digestive gland; HD, hermaphroditic duct; LCe, left cerebral ganglion; OT, ovotestis; P, proximal; RCe, right cerebral ganglion; RPa, right parietal ganglion; SV, seminal vesicle; V, visceral ganglion.

View larger version (26K): [in a new window]   Fig. 4. Effect of ovotestis (OT) mechanical stimulation on the frequency of afferent spikes in the intestinal nerve. (A) Representative traces from three electrodes placed on the intact nerve (see Fig. 1). A wooden applicator stick mounted on a micro manipulator was used to gently stroke the surface of the OT for 3 s; arrow indicates the onset of stimulation. (B) A representative portion of the record from A is amplified to illustrate the discrimination of efferent spikes (open arrowheads) and afferent spikes (filled arrowheads) based on inter-spike intervals recorded at distal and proximal electrodes positioned along the seminal vesicle; signals recorded at the central electrode were not used for this purpose. (C) Raster plot showing the timing of afferent spike activity for 30 s periods before and after the stimulus. The arrow at time 0 indicates the onset of mechanical stimulation.

View larger version (164K): [in a new window]   Fig. 2. Innervation of the ovotestis (OT) in Helix aspersa. (A) Wholemount of the OT embedded within the digestive gland. The dotted line delineates the perimeter of the OT. Neurobiotin was applied to the cut end of the intestinal nerve in this preparation (note the darkened stump), and the oocytes reacted nonspecifically to the histochemical procedure used to visualize the nerve. (B) Magnification of a portion of the hermaphroditic duct and OT from A showing fine branching in the intestinal nerve. (C) Frozen section (20 µm) from a second preparation showing innervation (arrows) along the wall of an acinus. Scale bars: A, 1 mm; B, 550 µm; C, 170 µm.

View larger version (110K): [in a new window]   Fig. 3. Electron micrographs of the intestinal nerve in cross section. (A) Section of the nerve at the level of the seminal vesicle. There are 3025 fibre profiles, of which 1732 (57%) have diameters <0.20 µm. (B) Enlargement of the boxed area in A showing the region of very small diameter fibres. Note the surrounding boundary formed by processes of darkly staining glial cells (arrowheads).

View larger version (13K): [in a new window]   Fig. 5. Spiking activity in the intestinal nerve relative to the number of mature oocytes present in the ovotestis. (A) Recordings obtained from snails with large numbers of mature oocytes had afferent spike rates substantially higher than those recorded in snails with few mature oocytes. Data points are means ± S.E.M. for five randomly selected periods of 1 min duration. Diggers were observed excavating nests within 5 days prior to the recordings. The number of deposited eggs was determined from our laboratory colony (mean = 86.9±2.7, N=104). (B) Log transformation of the data shown in A. The line is the linear regression (r2=0.812, P<0.001, N=14). (C) Log-transformed data showing the relationship between afferent spike rates and efferent spike rates (r2=0.623, P<0.001, N=14).

View larger version (26K): [in a new window]   Fig. 6. Effect of ovotestis (OT) inflation on afferent spike frequencies in the intestinal nerve. (A) Representative recordings obtained 10 s after injecting saline at incremented levels of OT inflation. Below each trace is a raster plot showing the timing of afferent spikes. (B) Quantification of afferent spike frequencies from the traces shown in A.

View larger version (48K): [in a new window]   Fig. 7. Mechanical stimulation of the ovotestis induces an efferent reflex response from the CNS that travels into both the pericardial (PC) and ovotestis branches of the intestinal nerve. (A) Traces recorded at four positions on the intestinal nerve (see Fig. 1). Action potentials conducted to and from the ovotestis were recorded by two electrodes (SV-P and SV-D) placed on the nerve as it passes over the seminal vesicle; afferent vs efferent spikes were discriminated using timing differences at these two electrodes. The arrowhead indicates stimulation of the ovotestis with a wooden applicator stick (3 s duration). Note that an elevated level of activity is recorded at all electrodes in the 10 min period following the stimulus. (B) Raster plot showing the timing of afferent and efferent spikes recorded at seminal vesicle electrodes as well as efferent activity recorded at the pericardial electrode. Time 0 indicates the onset of tactile stimulation.

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