Memories are vulnerable to disruption following a learning
experience until they become stabilized through processes
beginning during the learning phase and extending for a few
hours afterward. That is, memory is labile until it undergoes
the consolidation process (Lechner et al., 1999; McGaugh,
2000). Memory can be characterized in a number of different
ways, one being for how long the memory persists. Thus
memory can be divided into short (STM), intermediate (ITM)
and long-term (LTM) forms. STM persists for only a few
minutes while the longer lasting ITM and LTM persist for
hours, days, weeks and years. ITM endures for only a few
hours, while LTM survives for at least 1 day. The cellular,
biochemical and molecular differences underlying these two
forms of long-lasting memory are not completely understood
(Squire and Kandel, 1999; Kandel and Pittenger, 1999). Most
of the recent studies on formation and persistence of memory
have focused on neural analogues of STM and LTM (Lechner
et al., 1999; Martin et al., 2000). At both the behavioural and
neuronal levels, however, far less attention has been paid to the
shorter-lasting form of LTM, which was termed ITM in 1993
by Rosenzweig et al. (1993) (Lukowiak et al., 2000; Sutton et
al., 2001).
The variation in the length of perseverance between ITM
and LTM is most likely due to important molecular
dissimilarities that underlie their encodement. Chief among
these differences is the necessity for the transcription process.
While both ITM and LTM require new protein synthesis, only
LTM requires the transcription process. That is, LTM requires
both altered gene activity and protein synthesis, while ITM
requires only the translation process (Davis and Squire, 1984;
Rosenzweig et al., 1993; McGaugh, 2000). Data obtained so
far strongly support the idea that there are evolutionarily
conserved mechanisms underlying LTM formation. They
appear to involve both a cAMP-dependent MAP kinase signal
transduction cascade culminating in the activation of CREB
transcription factors (Tully, 1998; Mayford and Kandel, 1999;
Silva et al., 1998) and formation of the CCAAT enhancer
binding protein (C/EBP; Alberini et al., 1994; Taubenfeld et
al., 2001).
Far less is known about the molecular basis underlying ITM.
Prior to the discovery of a memory component of intermediate
duration dependent upon different classes of protein kinase
activities than those required for LTM (Rosenzweig, 1993), it
was widely believed that ITM was indistinguishable from
LTM. These shorter-lasting forms of memory have since
been distinguished at a behavioural level through classical
conditioning of Aplysia feeding behaviour (Botzer et al., 1998)
and sensitization of the siphon withdrawal response (a form of
non-associative learning; Sutton et al., 2001), as well as
through operant conditioning of aerial respiration in Lymnaea
(Lukowiak et al., 2000). At the neuronal level, analogues of
ITM have been demonstrated at both Aplysia and Hermissenda
CNS synapses where synaptic transmission is facilitated
(Ghirardi et al., 1995; Crow et al., 1999; Sutton et al., 2001).
1605 The Journal of Experimental Biology 206, 1605-1613
© 2003 The Company of Biologists Ltd
doi:10.1242/jeb.00301
Aerial respiratory behaviour in the pond snail, Lymnaea
stagnalis, can be operantly conditioned. This associative
learning then undergoes consolidation into a long-lasting
memory which, depending on the training procedure used,
causes intermediate-term memory (ITM; lasting 3·h) or
long-term memory (LTM; lasting >6·h) to be formed. We
determined the differential susceptibility of these two
forms of memory to translation and transcription
blockers. The injection of a translation blocker,
Anisomycin, 2.5·h before training prevents the
establishment of both ITM and LTM. On the other hand,
injection of the transcription blocker Actinomycin D, 2.5·h
before training, did not prevent the establishment of ITM,
but did, however, prevent LTM formation. Thus in
Lymnaea, following associative learning, both ITM and
LTM are dependent on new protein synthesis. ITM
appears to be dependent on protein synthesis from pre-
existing transcription factors, whilst LTM is dependent on
protein synthesis from new transcription messages.
Key words: Lymnaea stagnalis, intermediate memory, long-term
memory, protein synthesis, associative learning.
Summary
Introduction
Intermediate and long-term memories of associative learning are differentially
affected by transcription versus translation blockers in Lymnaea
Susan Sangha, Andi Scheibenstock, Chloe McComb and Ken Lukowiak*
Department of Medical Physiology and Biophysics, Neuroscience Research Group, 3330 Hospital Drive NW,
University of Calgary, Calgary, Alberta T2N 4N1, Canada
*Author for correspondence (e-mail: lukowiak@ucalgary.ca)
Accepted 18 February 2003