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Articles, Behavioral/Cognitive

AKAPS Act in a Two-Step Mechanism of Memory Acquisition

Lisa Scheunemann, Philipp Skroblin, Christian Hundsrucker, Enno Klussmann, Marina Efetova and Martin Schwärzel
Journal of Neuroscience 30 October 2013, 33 (44) 17422-17428; https://doi.org/10.1523/JNEUROSCI.1303-13.2013
Lisa Scheunemann
1Free University Berlin, Biology-Genetics, D-14195 Berlin, Germany and
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Philipp Skroblin
2Max-Delbrück-Centrum für Molekulare Medizin, 13125 Berlin, Germany
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Christian Hundsrucker
2Max-Delbrück-Centrum für Molekulare Medizin, 13125 Berlin, Germany
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Enno Klussmann
2Max-Delbrück-Centrum für Molekulare Medizin, 13125 Berlin, Germany
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Marina Efetova
1Free University Berlin, Biology-Genetics, D-14195 Berlin, Germany and
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Martin Schwärzel
1Free University Berlin, Biology-Genetics, D-14195 Berlin, Germany and
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    Figure 1.

    Independent contribution of shock number and intensity to reinforcement. Aversive olfactory conditioning induces associative memories that guide behavior in subsequent test situations and immediately after the training session animals perform due to STM. A, In the standard training situation originally introduced by Tully and Quinn (1985) animals are presented one particular odor of an odor pair while experiencing inevitable electric shock punishment that is administered in fast succession, followed by the unpunished control odor. To exclude unspecific odor effects the identity of punished and control odor—in this study IAA and EA—is exchanged in two separate experiments and both groups are tested in a similar situation for odor preference using a forced choice maze. The percentage of correct choice, i.e., avoidance of the formerly punished odor, is averaged from both experiments and interpreted as memory performance. B, For modulation of shock number we varied the number of shocks applied during the training procedure. Shock impact was set to 15 V, 30 V, 60 V, or 120 V DC. C, Performance of STM is plotted against the different combinations of shock number and impact used for training. Each bar represents the mean of 6–8 biological repetitions. D, STM performance of dnc1 mutants plotted against shock number as experienced during training sessions with 120 V DC. E, STM performance of rut1 mutants plotted against shock iteration as experienced during training sessions with 120 V DC. F, STM performance of wild-type Canton-S plotted against shock number as experienced during training sessions with 120 V DC. Error bars indicate the mean ± SEM 6–8 biological repetitions, i.e., N = 6–8. Statistical differences at level of p ≤ 0.05 are denoted by different letters. Note that false colors are intended to improve clarity of each part and are not matched between parts.

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    Figure 2.

    Distinct acquisition dynamics of consolidated and labile memories. At 3 h after training memory is proportionally supported by consolidated ARM and labile ASM. Shock impact and/or number differently affect those distinct memory phases. A, Performance of consolidated ARM is independent from variation of shock number and impact used for training. B, Performance of labile ASM, in contrast, is doubly dependent on shock number and impact with repeated experience of high-impact reinforcement producing a characteristic “boost” in performance. C, Performance of MTM, i.e., the composite of labile ASM and consolidated ARM, is plotted against the different combinations of shock number and impact used for training. N = 6–8 for each bar.

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    Figure 3.

    Psychophysical characterization of an ASM filter. Formation of ASM is critically dependent on two consecutive shock iterations administered in an associative context. To determine temporal aspects critical for this type of memory acquisition we modulated the training procedure to present short (10 s) puffs of odor in combination with electric shock. Those CS/US pairings could be repeated at various ITIs (see inlay). Performance of ARM is indicated by gray symbols. A, Formation of ASM is dependent on a critical ITI in between two consecutive CS/US pairing that can last for up to 300 s. B, ASM formation requires an associative context, i.e., contingent presentation of CS and US, during either of the two conditioning trials. C, High shock impact, i.e., >120 V DC, is required during either of the consecutive trials. Each error bar indicates the mean ± SEM 6–8 biological repetitions. Statistical differences at the level of p ≤ 0.05 are denoted by different letters.

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    Figure 4.

    Rut-AC1 supports step-like ASM formation at the KC layer. Labile ASM and consolidated ARM are plotted against the increasing number of shock iterations experienced during training sessions with 120 V DC. A, Wild-type Canton-S shows characteristic stepwise acquisition of ASM. B, rut1 mutants do not form ASM. C, Genetic rescue of Rut-AC1 function within KCs marked in the mb247-Gal4 line is sufficient to restore two-step ASM formation. D, E, Genetic controls that bear either UAS-rut+ or mb247-Gal4 in rut1 mutant background alone did not improve ASM. F–J, Instantaneous formation of ARM is independent from rut1 mutant background. Error bars indicate the mean ± SEM 6–8 biological repetitions. Statistical differences at level of p < 0.01 are denoted by asterisks (**).

  • Figure 5.
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    Figure 5.

    Step-like ASM formation requires AKAPs at the KC layer. Labile ASM and consolidated ARM are plotted against the increasing number of shock iterations experienced during training sessions with 120 V DC. A, Wild-type Canton-S shows characteristic stepwise acquisition of ASM. B, Expression of the ecopr2 peptide competitor that disrupts PKA–AKAP interaction prevents formation of ASM. Expression was restricted to KCs by use of the mb247-Gal4 line. C, D, Genetic controls that bear either ecopr2 or mb247-Gal4 alone did not affect ASM. E–H, Instantaneous formation of ARM is unaffected in those genotypes. Error bars indicate mean ± SEM 6–8 biological repetitions. Statistical differences at level of p < 0.01 are denoted by asterisks (**).

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The Journal of Neuroscience: 33 (44)
Journal of Neuroscience
Vol. 33, Issue 44
30 Oct 2013
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AKAPS Act in a Two-Step Mechanism of Memory Acquisition
Lisa Scheunemann, Philipp Skroblin, Christian Hundsrucker, Enno Klussmann, Marina Efetova, Martin Schwärzel
Journal of Neuroscience 30 October 2013, 33 (44) 17422-17428; DOI: 10.1523/JNEUROSCI.1303-13.2013

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AKAPS Act in a Two-Step Mechanism of Memory Acquisition
Lisa Scheunemann, Philipp Skroblin, Christian Hundsrucker, Enno Klussmann, Marina Efetova, Martin Schwärzel
Journal of Neuroscience 30 October 2013, 33 (44) 17422-17428; DOI: 10.1523/JNEUROSCI.1303-13.2013
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