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First published online May 1, 2006
Journal of Experimental Biology 209, 1976-1987 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02224

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The effects of temperature on peripheral neuronal function in eurythermal and stenothermal crustaceans

John S. Young^1,*, Lloyd S. Peck² and Thomas Matheson^1,

¹ Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK
² British Antarctic Survey, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

View larger version (35K): [in a new window]   Fig. 1. (A) The neuronal conduction velocity of axons in the leg nerves of marine crustaceans increases with temperature. Electrical stimulation of the leg nerve at a proximal site produces a stimulus artefact (black arrowheads), and compound action potentials recorded at a distal site, the most rapid of which are indicated by open arrowheads. Traces are aligned to the stimulus artefact, indicated by the first broken line in each block. The first peak of the compound action potential occurs sooner as temperature increases (second broken line). Scale bar, 5 ms. (B,C) Increasing the stimulation voltage reveals a sharp threshold for eliciting a compound action potential (B), which does not change with temperature(C). Increasing the stimulus voltage further results in only a modest increase in the measured conduction velocity (B). The arrow indicates 130% of threshold, which is the stimulation level used throughout this study. Data in B are from one experiment in G. antarcticus. Data in C are from five experiments in G. antarcticus, denoted by different symbol types. Regression equation: y=–1.93x10–3x+1.266, r2=0.033, P=NS.

View larger version (35K): [in a new window]   Fig. 2. (A–D) The effect of temperature on the neuronal conduction velocity of (A) C. maenas (N=6), (B) G. antarcticus (N=7), (C) L. oceanica (N=7) and (D) P. gibber (N=6). The different symbols denote different animals. Data extend across the full range of temperatures at which action potentials were elicited by electrical stimulation. Note the different scale in A. (E) There is a differential effect of temperature on the neuronal conduction velocity of four species of marine crustacean. Conduction velocity is derived from the mean conduction velocity per animal per 1°C temperature bin. Values are means ± s.e.m. For L. oceanica, G. antarcticus and P. gibber, the number of animals (N) was at least 5 except for the following temperature bins: L. oceanica; –1.5°C (N=2), –0.5 and +0.5°C (N=3), +1.5°C (N=2), +2.5°C (N=3), and +19.5°C (N=3).G. antarcticus; –2.5°C (N=1), +8.5°C (N=4), +10.5°C (N=4), +12.5°C (N=4), +15.5°C (N=4), +17.5°C (N=3), +18.5 and +19.5°C (N=4), +20.5 and +21.5°C (N=1). P. gibber; +6.5°C (N=4), +15.5°C (N=4), +17.5 and +18.5°C (N=4), and +19.5°C (N=1). For C. maenas, the number of animals was at least 3 except for the following temperature bins: Group A; –2.5 to –0.5°C (N=1), +0.5°C (N=2), +12.5°C (N=2), +16.5°C (N=2), and +20.5°C to +22.5°C (N=2). Group B; –1.5°C (N=2), +18.5°C (N=2), and +22.5°C (N=1). (F) Conduction velocity of sensory action potentials, elicited by moving single spines on the carpus or merus of G. antarcticus. Larger amplitude action potentials conducted more rapidly (solid symbols and solid lines) than the smaller amplitude ones (open symbols and broken lines), but their temperature dependence was similar to one another and to that of the compound potential recorded from the whole nerve. These data come from experiments on four spines in two animals. Animal 1: spine A, merus (circles), spine B, merus (squares) and spine C, carpus (triangles). Animal 2: spine D, merus (solid diamonds).

View larger version (24K): [in a new window]   Fig. 3. (A) Changes of temperature have a greater effect on the neuronal conduction velocity of axons in the leg nerve of C. maenas than in the other three crustacean species (Kruskal–Wallis, 2=13.36, P<0.01). (B) Conduction velocity at 2°C is greater in C. maenas (Kruskal–Wallis, 2=19.55, P<0.0001) than in the other species. Slopes and intercepts were calculated by performing a linear regression on the temperature vs conduction velocity for each animal of each species. The N values are the number of animals per species used. Each boxplot shows the median value, the upper and lower quartiles and the minimum and maximum values. Outliers, which are either 1.5–3 times or >3 times the interquartile range from the quartiles, are denoted by a circle or an asterisk, respectively. The conduction velocity and thermal dependence of conduction velocity of sensory neurones in two G. antarcticus (G. a. sensory) were similar to values for the whole nerve. We acclimated two additional G. antarcticus to 4°C for 7 days before measuring leg nerve conduction velocity (G. a. acclim.). These values (solid circles) lie within the range for animals acclimated to 0–1°C (A,B). The light grey shading groups together all the values from G. antarcticus.

View larger version (31K): [in a new window]   Fig. 4. (A) In G. antarcticus (N=2), moving individual articulated spines on the leg (black bar) produced bursts of action potentials recorded in the leg nerve. (B) The number of action potentials elicited by each touch depended on the temperature. Values are mean ±1 s.d.

View larger version (74K): [in a new window]   Fig. 5. (A) Composite transmission electron micrograph of a transverse section through one nerve bundle of the leg nerve within the basis of G. antarcticus. (B) The lines show the measured diameter of each axon. Scale bar, 10 µm.

View larger version (15K): [in a new window]   Fig. 6. The frequency distribution of axons of 0–10 µm diameter within the basal leg nerve of L. oceanica (A) and G. antarcticus (B). Insets show the frequency distributions for axons of 10–30 µm diameter. The filled circles are values for N=2 animals of each species; the grey bars are the mean frequencies for each species.

View larger version (162K): [in a new window]   Fig. 7. A nerve bundle of G. antarcticus containing axons (a) surrounded by a wrapping (black arrowhead). The appearance of the axonal wrapping is very different from the sheath that surrounds the nerve bundle (white arrowhead). The nerve bundle contains substantial interstitial spaces (*). The dark blotches are staining artefacts. Scale bar, 10 µm.

View larger version (21K): [in a new window]   Fig. 8. The effect of temperature on the conduction velocity of identified neurones or nerves of invertebrates, from this study [C. maenas (C.m. A, C.m. B), L. oceanica (L.o.), G. antarcticus (G.a.) and P. gibber (P.g.); open symbols) and published data (solid and grey symbols]. Key: 1squid Loligo vulgaris, motor neurone (MN) (Chapman, 1967); 2spider Cupiennius salei, sensory neurone (SN) (Höger and French, 1999); 3cockroach Periplaneta americana, SN (Chapman and Pankhurst, 1967); 4locust Locusta migratoria MN (Xu and Robertson, 1994); 5locust Locusta migratoria interneurone (IN) (Money et al., 2005); 6locust Schistocerca gregaria (MN) (Burrows, 1989); 7G. antarcticus, ventral nerve cord and leg nerve recordings combined (Macdonald, 1981), 8C. maenas, SN (Fraser, 1990) and 9Colossendeis robusta, leg nerve recordings (Macdonald, 1981).