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Gone but not forgotten: the lingering effects of intermediate-term memory on the persistence of long-term memory

Kim Smyth, Susan Sangha and Ken Lukowiak^*

Department of Physiology and Biophysics, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada T2N 4N1

View larger version (11K): [in a new window]   Fig. 1. The intermediate-term memory (ITM) training procedure results in learning and a memory that persists for 3 h but not for 4 h. (A) A cohort of 20 naïve snails received three 15 min operant conditioning training sessions, with each training session separated by a 30 min rest interval. Learning occurred (ANOVA, F19,2=9.1613, P<0.001); session 3 was significantly different from session 1 (P<0.01). Memory was tested 3 h later (memory test, MT; cross-hatched column). There was no significant difference in the response between the MT and session 3 (NSD, P>0.05), but there was a significant difference between the response in session 1 and MT (P<0.01). (B) As in A, except that the MT was presented 4 h after session 3 (N=20). Learning occurred (ANOVA, F19,2=15.7055, P<0.001); session 3 was significantly different from session 1 (P<0.01). There was no memory 4 h after the last training session. There was a significant difference between the response in session 3 and MT (P<0.01), but there was no significant difference between the response in session 1 and MT (NSD, P>0.05).

View larger version (32K): [in a new window]   Fig. 2. The long-term memory (LTM) training procedure results in learning and memory that persists for 48 h but not for 72 h. (A) A cohort of 20 naïve snails received three 15 min operant conditioning training sessions, with each training session separated by a 1 h rest interval. Learning occurred (ANOVA, F19,2=9.7738, P<0.001); session 3 was significantly different from session 1 (P<0.01). Memory was tested 48 h later (memory test, MT; cross-hatched column). There was no significant difference between the response in the MT and that in session 3 (NSD, P>0.05), but there was a significant difference between the response in session 1 and that in the MT (P<0.01). (B) As in A, except that the memory test (MT) was presented 72 h after session 3 (N=20). Learning occurred (ANOVA, F19,2=11.4214, P<0.001); session 3 was significantly different from session 1 (P<0.01). There was no memory 72 h after the last training session. There was a significant difference between the response in session 3 and that in the MT (P<0.01), but there was no significant difference between the response in session 1 and that in the MT (NSD, P>0.05).

View larger version (22K): [in a new window]   Fig. 3. Previous intermediate-term memory (ITM) training does not negatively affect the ability to form long-term memory (LTM). (A) A cohort of 20 naïve snails received three 15 min operant conditioning training sessions, with each training session separated by a 30 min rest interval. Learning occurred (ANOVA, F19,2=12.1514, P<0.001); session 3 was significantly different from session 1 (P<0.01). Following a 3 h rest interval, these snails received the LTM training procedure, and memory was tested 48 h after the last LTM training session. The number of attempted pneumostome openings in session 4 was not significantly different (NSD, P>0.05) from that in session 3, indicating that ITM was present. The LTM training procedure resulted in no further statistically significant decrease in the number of attempted openings (session 4 was not significantly different from session 6, P>0.05). Memory was present when tested 48 h later because the memory test (MT) was not significantly different from session 6 (NSD, P>0.05), but was significantly different from session 1 (P<0.01). (B) As in A except that the LTM training procedure was initiated 4 h after the last ITM training session. Note that there was a significant difference between the response in session 3 and that in session 4 (P<0.01), indicating that there was no ITM. The previous ITM training did not interfere with the establishment of LTM at 48 h because MT was not significantly different from session 6 (NSD, P>0.05), but was significantly different from session 1 (P<0.01).

View larger version (17K): [in a new window]   Fig. 4. Previous intermediate-term memory (ITM) training augments long-term memory (LTM) retention if LTM training occurs up to 5 h after the final ITM training session. A cohort of 20 naïve snails received ITM training and, as in Fig. 3A, exhibited memory at 3 h: the number of attempted pneumostome openings in session 4 was not significantly different (NSD, P>0.05) from that in session 3. Following this interval, these snails received the LTM training procedure and memory was tested 72 h after the last LTM training session. The LTM training procedure resulted in no further statistically significant decrease in the number of attempted openings: session 4 was not significantly different from session 6 (P>0.05). Memory was present when tested 72 h later because the memory test (MT) was not significantly different from session 6 (NSD, P>0.05), but was significantly different from session 1 (P<0.01). (B) As in A, except that the LTM training procedure was initiated 5 h after the last ITM training session. Note that there was a significant difference between the response in session 3 and that in session 4 (P<0.01), indicating that there was no ITM. Memory was present when tested 72 h later because MT was not significantly different from session 6 (NSD, P>0.05), but was significantly different from session 1 (P<0.01). (C) As in A, except that the LTM training procedure was initiated 8 h after the last ITM training session. In this group of snails, there was no augmentation of LTM. That is, there was a significant difference between session 6 and MT (P<0.01) but no significant difference between MT and session 1 (NSD, P>0.05), indicating no memory at 72 h. (D) As in C, except that the LTM training procedure was initiated 24 h after the last ITM training session. Again, there was no augmentation of LTM. There was a significant difference between session 6 and MT (P<0.01) but no significant difference between MT and session 1 (NSD, P>0.05), indicating no memory at 72 h.

View larger version (26K): [in a new window]   Fig. 5. Yoked controls do not show augmentation of long-term memory (LTM) retention. (A) A cohort of 15 naïve snails received three yoked control intermediate-term memory (ITM) training sessions. Three hours later, they received the LTM training procedure. Learning was evident (ANOVA, F14,2=15.2849 P<0.0001; session 6 was significantly different from session 4, P<0.01), but memory was not present when tested 72 h after the last LTM training session: there was a significant difference between session 6 and the memory test (MT) (P<0.01) but no significant difference between MT and session 4 (NSD, P>0.05). (B) Another naïve cohort of snails (N=15) received three yoked control ITM training sessions. Eight hours later, they received the LTM training procedure. Learning was evident (ANOVA, F14,2=11.7037 P<0.0002; session 6 was significantly different from session 4, P<0.01) but memory was not present when tested 72 h after the last LTM training session: there was a significant difference between session 6 and MT (P<0.01) but no significant difference between MT and session 4 (NSD, P>0.05).

View larger version (20K): [in a new window]   Fig. 6. Extinction training following intermediate-term memory (ITM) training prevents the augmentation of memory retention. (A) A cohort of 20 naïve snails received the ITM training procedure as in Fig. 1. Following a 2 h rest interval, these snails received extinction training (AE) before receiving the long-term memory (LTM) training procedure. Note that extinction training obliterated ITM. That is, the number of attempted pneumostome openings in session 4 was significantly different from that in session 3 (P<0.01) and was not significantly different from that in session 1 (P>0.05). The LTM training procedure resulted in a memory that persisted for 48 h. That is, the memory test (MT) was not significantly different from session 6 (NSD, P>0.05), but was significantly different from session 1 (P<0.01). (B) As in A, except that LTM was tested 72 h after the last LTM training session. Memory was not present because there was a significant difference between session 6 and MT (P<0.01) but no significant difference between MT and session 1 (NSD, P>0.05).

View larger version (19K): [in a new window]   Fig. 7. Repeated intermediate-term memory (ITM) training by itself does not result in long-term memory (LTM). (A) A cohort of naïve snails (N=15) received six ITM training session (i.e. 15 min sessions separated by a 30 min rest interval). Learning was evident (ANOVA, F14,5=14.2849, P<0.0001): session 6 was significantly different from session 1 (P<0.01); but memory was not present when tested 72 h later. That is, there was a significant difference between session 6 and the memory test (MT) (P<0.01) but no significant difference between MT and session 1 (NSD, P>0.05). (B) A naïve cohort of snails (N=20) first received three ITM training sessions and then, following a 4 h interval, received a further three ITM training sessions. In each sequence of ITM training, learning was observed (ANOVA, F19,2=12.171, P<0.0001, in the first sequence; ANOVA, F19,2=10.09, P<0.0003, in the second sequence). However, when LTM was tested 72 h after the last ITM training session (session 6), no memory was observed; i.e. MT was significantly different from session 6 (P<0.01) but was not significantly different from session 4 or session 1 (NSD, P>0.05 in both cases).