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First published online August 22, 2008
Journal of Experimental Biology 211, 2807-2816 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.020172

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Comparing memory-forming capabilities between laboratory-reared and wild Lymnaea: learning in the wild, a heritable component of snail memory

Michael V. Orr, Karla Hittel and Ken Lukowiak^*

Hotchkiss Brain Institute, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada, T2N 4N1

View larger version (125K): [in this window] [in a new window]   Fig. 1. (A) Laboratory-reared snail performing aerial-respiratory behavior at the air–water interface. Note that the markings on the dorsal shell are utilized in the laboratory for identifications purposes. (B) A wild Lymnaea stagnalis aerial-respiring in its native habitat. The bars indicate that the wild snail is approximately twice the size of the laboratory snail.

View larger version (15K): [in this window] [in a new window]   Fig. 2. Behavioral response of wild Belly (left black bars) and laboratory snails (descendents of wild Dutch snails; right white bars) after a single 0.5 h training session (TS). (A) Operant conditioning of wild Belly snails results in an LTM that persists for 24 and 72 h (24 h TM, N=53, P<0.05; 72 h TM, N=23, P<0.05). Yoked control snails do not demonstrate memory at these same time periods (faded bars; 24 h yoke, N=26, P=0.36; 72 h yoke, N=25, P=0.45). Snails did not demonstrate memory after 1 week (1 week TM, N=32, P=0.24). (B) Laboratory snails do not demonstrate LTM after a single 0.5 h training session (TS; 24 h TM, N=30, P=0.55; 24 h yoke, N=15, P=0.42). All results shown as means + s.e.m. **P<0.001.

View larger version (6K): [in this window] [in a new window]   Fig. 3. Behavioral response of wild Dutch snails after a single 0.5 h training session (TS). Wild Dutch snails do not demonstrate LTM when tested 24 h after operant conditioning (left light-gray bars, 24 h TM, N=22, P=0.60). Yoked controls do not demonstrate altered behavior after conditioning (right faded-black bar, 24 h yoked, N=16, P=0.57). Results are shown as means + s.e.m.

View larger version (11K): [in this window] [in a new window]   Fig. 4. Behavioral response of Belly F1 snails after a single 0.5 h training session (TS). Operant conditioning of Belly F1 snails results in an LTM that persists for 24 and 72 h (24 h TM, N=26, P<0.05; 72 h TM, N=26, P<0.05). Yoked control snails do not demonstrate memory at these same time periods (faded-black bars, 24 h yoke, N=24, P=0.55; 72 h yoke, N=25, P=0.73). Snails did not demonstrate memory after 1 week (1 week TM, N=25, P=0.82). Results are shown as means + s.e.m. **P<0.001.

View larger version (28K): [in this window] [in a new window]   Fig. 5. Representative electrophysiological recordings from RPeD1 in semi-intact preparations taken from wild Dutch and laboratory snails before (naive) and 24 h after operant conditioning. No significant differences were found between any of the measured electrophysiological characteristics (wild Dutch naive, N=8; wild Dutch 24 h, N=8; laboratory-reared Dutch naive, N=9; laboratory-reared Dutch 24 h, N=8).

View larger version (48K): [in this window] [in a new window]   Fig. 6. RPeD1 activity in wild Belly snails following the single 0.5 h training session. (A) Representative recordings from RPeD1 in wild Belly snails starting at top with a naive snail (naive wild Belly), 24 h after the operant conditioning procedure, 72 h after conditioning, 72 h yoked control and 1 week after conditioning. (B) Summary data for mean (+s.e.m.) spiking activity per 600 s. (C) Number of spikes per burst. (D) Burst duration. (E) Number of bursts per 600 s. In all measured characters presented here, both the 24 h and 72 h operantly conditioned groups demonstrated significantly lower activity than the naive state and are significantly lower than the 72 h yoke and 1 week groups. 72 h yoke and 1 week groups are not significantly different from the naive state. All data represent log-transformed values. *P<0.05; **P<0.001. Naive N=9; 24 h N=9; 72 h N=7; 72 h yoke N=7; and 1 week N=8. No significant differences were detected between treatments in other electrophysiological parameters measured (see Materials and methods).

View larger version (52K): [in this window] [in a new window]   Fig. 7. RPeD1 activity in Belly F1 snails following the single 0.5 h training session (A) Representative recordings from RPeD1 in Belly F1 snails starting at top with a naive snail (naive Belly F1), 24 h after the operant conditioning procedure, 72 h after conditioning, 72 h yoked control and 1 week after conditioning. (B) Summary data for mean (+s.e.m.) spiking activity per 600 s. (C) Number of spikes per burst. (D) Burst duration. (E) Number of bursts per 600 s. In all measured characters presented here, the 24 h and 72 h operantly conditioned groups both demonstrated significantly lower activity than the naive state (except burst duration at 72 h) and are significantly lower than the 72 h yoke and 1 week groups. 72 h yoke and 1 week groups are not significantly different from the naive state. All data represent log-transformed values. *P<0.05; **P<0.001. Naive N=8; 24 h N=7; 72 h N=7; 72 h yoke N=8; and 1 week N=7. No significant differences were detected between treatments in other electrophysiological parameters measured (see Materials and methods).

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