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First published online May 19, 2008
Journal of Experimental Biology 211, 1747-1756 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014886

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The perception of stress alters adaptive behaviours in Lymnaea stagnalis

Ken Lukowiak^*, Kara Martens, David Rosenegger, Kim Browning, Pascaline de Caigny and Mike Orr

Hotchkiss Brain Institute, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada, T2N 4N1

View larger version (9K): [in this window] [in a new window]   Fig. 1. The `Yerkes-Dodson law' is derived from experiments performed in the early 1900s and as plotted here (left) demonstrates a relationship between stress or arousal and performance. That is, in this conceptual scheme memory formation gets better with increasing stress, but only to a certain point: when levels of stress become too high, the ability to form memory decreases. A similar curve (right) has been experimentally derived with increasing concentrations of KCl as a stressor in Lymnaea [reprinted from Martens et al. (Martens et al., 2007a), with permission from Elsevier]. Briefly, when a 5 mmoll–1 concentration of KCl was used in the bath, memory was not observed. With concentrations of KCl greater than 25 mmoll–1 memory was obtained, but the optimal concentration of KCl was 25 mmoll–1 as with increasing concentrations the resultant memory was not as robust.

View larger version (11K): [in this window] [in a new window]   Fig. 2. A KCl stressor enhances LTM formation in Lymnaea. Top, snails (N=20) that received one 30 min training session (TS) of contingent `poking' did not have a significant change in breathing behaviour when tested 24 h later (MT; top). Bottom, snails (N=38) that were exposed to 25 mmoll–1 KCl for 30–35s before a 30 min TS exhibited memory at 24 h (**P<0.01). When tested in carrot context (CT) the number of attempted pneumostome openings returned to naive levels (P>0.05), indicating context-specific memory. Snails that received KCl before training and were tested for savings at 48 h did not show memory. [Reprinted from Martens et al. (Martens et al., 2007a), with permission from Elsevier.]

View larger version (12K): [in this window] [in a new window]   Fig. 3. Controls for the KCl bath experiments. Top, snails (N=19) that were placed in pond water (PW) rather than the KCl bath before 30 min of training did not have memory at 24 h. Bottom, snails (N=12) that were exposed to KCl and then yoke (i.e. non-contingently) trained showed no significant difference in the number of attempted pneumostome openings from naive levels, demonstrating that LTM was not formed. Reprinted from Neurobiology of Learning and Memory 87, 391–403 (2007) with permission from Elsevier (Martens et al., 2007a).

View larger version (4K): [in this window] [in a new window]   Fig. 4. A stressful event, the KCl bath, can improve memory at the time of recall. Snails (N=20) that were trained for 30 min and then only received KCl exposure before the memory test (MT) 24 h later exhibited memory when tested (*P<0.05). [Reprinted from Martens et al. (Martens et al., 2007a), with permission from Elsevier.]

View larger version (10K): [in this window] [in a new window]   Fig. 5. The soma of RPeD1 is required for memory formation with the KCl bath training procedure. Snails (N=22) that had the soma of RPeD1 ablated 2 days before training were placed in a 25 mmoll–1 KCl bath and then trained for 30 min (TS). A day later (MT) the number of attempted pneumostome was statistically the same as in TS. Thus LTM was not formed. On the other hand, snails (N=14) that had the soma of VD1 ablated 2 days prior to training did have memory at 24 h (**P<0.01).

View larger version (10K): [in this window] [in a new window]   Fig. 6. Too much stress and LTM formation. Snails that received a 30–35s KCl bath before 30 min of tactile training, and then another 30–35s KCl bath afterwards, did not have a significant decrease in pneumostome openings in a MT 24 h later. When snails had the KCl bath and then training, but had the second KCl bath replaced with exposure to pond water (PW) there was memory, i.e. there was a significant decrease in attempted openings, 24 h later (**P<0.01). [Reprinted from Martens et al. (Martens et al., 2007a), with permission from Elsevier.]

View larger version (9K): [in this window] [in a new window]   Fig. 7. Crayfish effluent detection alters the righting response in Lymnaea. The change in mean (±s.e.m.) righting response time after exposure to pond (PW), crayfish (CE) or boiled crayfish effluent (BC) water (N=36). PW and BE means are not significantly different from each other (P>0.05) but are significantly different (*P<0.05) from CE treatment (repeated measures ANOVA) (from Orr et al., 2007).

View larger version (18K): [in this window] [in a new window]   Fig. 8. CE exposure, time to explore and shadow responses. Top, the mean (±s.e.m.) time to explore for snails placed in PW after a 2 h exposure to PW, CE or BC. Time to begin to explore in the CE treatment was significantly longer compared with snails in PW and snails in BC treatment (N=54, *P<0.001, one-way ANOVA). Bottom, snails in CE elicited full pneumostome withdrawal significantly more often when presented with a passing shadow than did snails in PW or BC (from Orr et al., 2007).

View larger version (26K): [in this window] [in a new window]   Fig. 9. Exposure to CE and aerial respiratory behaviour. The mean (±s.e.m.) number of pneumostome openings (A), total breathing time (B) and mean breathing time (C) of snails in each of the three water treatments. (A) Number of pneumostome openings in PW compared with that in CE and BC. The number for CE is significantly higher (*P<0.01, N=65) than that for either PW or BC, which were not significantly different from each other. (B) The total breathing time in PW, CE and BC (N=65). Again, CE results were significantly higher (**P<0.001) than those for either PW or BC, which were not significantly different from each other. (C) The mean breathing time was not significantly different in any of the groups (from Orr et al., 2007).

View larger version (51K): [in this window] [in a new window]   Fig. 10. CE exposure and RPeD1 activity in semi-intact preparations. (A) Representative electrophysiological recordings from RPeD1 in semi-intact preparations taken after intact snails were exposed to PW (top), CE (middle) or BC (bottom) treatments. All traces demonstrate spontaneous firing activity, and bursting activity. (B) Summary data for mean (±s.e.m.) spiking activity per 10 min (square-root transformed, N=14). Results for CE were significantly lower (**P<0.001, N=14) than those for either PW or BC, which were not significantly different from each other. (C) Mean (±s.e.m.) number of spikes per burst. Again, results for CE were significantly lower (**P<0.001, N=14) than those for either PW or BC, which were not significantly different from each other (from Orr et al., 2007).

View larger version (20K): [in this window] [in a new window]   Fig. 11. Behavioural data of intact Lymnaea after the single 0.5 h training procedure in either PW or CE. The single training session (TS1) in PW (black bars) results in a 3 h memory (3 h TM; intermediate-term memory, ITM) but does not result in LTM (i.e. a memory lasting 24 h; black bars, N=44, P>0.05). However, the single training session (TS1) in CE (orange) results in LTM. That is, the number of attempted pneumostome openings in the memory test sessions (TM) at 24 and 48 h is significantly lower than in TS1 (i.e. memory at 24 and 48 h; 24 h TM, N=35, *P<0.01; 48 h TM, N=41, *P<0.01). Snails did not demonstrate memory formation in 24 and 48 h yoked control groups (blue bars; N=30, P>0.05 and N=20, P>0.05 for 24 and 48 h yokes, respectively) or 72 h after training (N=22, P>0.05). [Reproduced with permission from Orr and Lukowiak (Orr and Lukowiak, 2008).]

View larger version (44K): [in this window] [in a new window]   Fig. 12. Representative electrophysiological recordings of RPeD1 from semi-intact animals after the single 0.5 h training session in either PW or CE. Representative recordings from RPeD1 in the naive state (untrained and in PW), 24 h post-PW single training session, 48 h after single training session in CE, 48 h CE single training session yoke control and 72 h after the single training session in CE. Right panels: top, summary data for mean (±s.e.m.) spiking activity per 600 s; middle, number of spikes per burst (all values log transformed). Results for the 48 h single training session procedure in CE are significantly lower than the naive state (N=7, **P<0.01). Results for 24 h single training session in PW trained animals, 48 h single training session in CE yoked and 72 h single training session in CE trained animals are not significantly different from the naive state (24 h PW single training session, N=8, P>0.05; 48 h CE single training session yoked, N=8, P>0.05; and 72 h CE single training session, N=6, P>0.05). Bottom bar graph demonstrates summary data for burst duration (mean ± s.e.m., values log transformed) of each treatment. Burst duration for single training session in CE at 48 h is significantly lower than in the naive state (N=7, P<0.05). Single training session in PW at 24 h, single training session in CE at 48 h yoked and single training session in CE at 72 h are not significantly different from the naive state (24 h PW single training session, N=8, P>0.05; 48 h CE single training session yoked, N=8, P>0.05; and 72 h CE single training session, N=6, P>0.05). [Reproduced with permission from Orr and Lukowiak (Orr and Lukowiak, 2008).]