The effects of continuous versus partial reinforcement schedules on associative learning, memory and extinction in Lymnaea stagnalis
Department of Physiology and Biophysics, University of Calgary,
Faculty of Medicine, 3330 Hospital Drive NW, Calgary, Alberta, Canada T2N
4N1
*
Contributed equally to this study
Author for correspondence (e-mail:
lukowiak{at}acs.ucalgary.ca
)
Accepted 1 February 2002
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Summary |
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Key words: operant conditioning, partial reinforcement, extinction, long-term memory, Lymnaea stagnalis
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Introduction |
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Different schedules of reinforcement are used in studies of operant
conditioning and memory of the association. A schedule of continuous
reinforcement (CR) involves 100 % contingency between the behaviour and the
reinforcement; that is, reinforcement is presented every time the animal
performs the behaviour. Partial reinforcement (PR), however, refers to any
schedule in which there is less than 100 % contingency so that there are
instances when the animal's behaviour is not reinforced. In some operant
learning experiments, PR may interfere with the initial acquisition of the
operant response, especially when a negative stimulus is used as the
reinforcing stimulus; in others, PR has been found to lead eventually to
superior performance (e.g. Weinstock,
1958).
If, following conditioning, animals receive extinction trials (in which
there is no reinforcement), the acquired association is lost, resulting in a
behavioural phenotype that resembles the naïve state
(Pavlov, 1927). The most
important variable determining the magnitude of the behavioural effects of an
extinction procedure is the schedule of reinforcement used in the acquisition
phase of learning (Domjan and Burkhard,
1993
). A PR-induced behaviour is more resistant to extinction than
a CR-induced behaviour. This phenomenon has been termed the partial
reinforcement extinction effect (PREE) and was first described in the work of
both Skinner and Humphreys in the late 1930s
(Skinner, 1938
;
Humphreys, 1939
). How can
partial, but not continuous, reinforcement offer resistance to extinction? One
suggestion proposed by Amsel
(1972
) is that a `disruptive
process', based on non-reward, emerges in partial reinforcement acquisition.
This disruptive process does not occur in ordinary CR training, so there is no
`counterconditioning'; extinction is therefore rapid after CR training. This
has sometimes been referred to as the `frustration theory'. Another
possibility is that, if the subject does not receive reinforcement after each
response during training, it may not immediately `notice' when reinforcement
ceases, as in extinction training. The change in reinforcement conditions is
more dramatic and noticeable if reinforcement ceases after continuous
reinforcement. This particular explanation of the PREE is called the
discrimination hypothesis (Domjan and
Burkhard, 1993
) and is somewhat similar to the PearceHall
model in that a PR schedule maintains attention because trial outcomes are
always `surprising' (Bouton and Sunsay,
2001
).
Operant conditioning protocols have been used in both vertebrates
(Chen and Wolpaw, 1995;
Feng-Chen and Wolpaw, 1996
) and
invertebrates (Horridge, 1962
;
Hoyle, 1980
;
Forman, 1984
;
Hawkins et al., 1985
;
Susswein et al., 1986
; Cook
and Carew,
1989a
,b
,c
;
Nargeot et al., 1997
). We have
studied operant conditioning of aerial respiratory behaviour in the freshwater
mollusc Lymnaea stagnalis
(Lukowiak et al., 1996
). The
advantage in using Lymnaea stagnalis as a model system for the study
of the neuronal basis of associative learning and its memory is that it has a
relatively simple behavioural repertoire and a relatively simple nervous
system that is easily accessible to neurophysiological analysis
(Spencer et al., 1999
;
Benjamin et al., 2001; Inoue et al.,
2001
). Lymnaea stagnalis is a pulmonate mollusc that
makes periodic visits to the water surface to replenish its air supply. It is
a bimodal breather that possesses a three-interneuron network whose necessity
and sufficiency have been demonstrated to mediate aerial respiratory behaviour
(Syed et al., 1990
,
1992
). Recently, we have
demonstrated neural correlates of associative learning and its memory in one
of the central pattern generator (CPG) neurons, RPeD1
(Spencer et al., 1999
).
Aerial respiration in Lymnaea stagnalis occurs at the water
interface and is achieved by opening and closing movements of its respiratory
orifice, the pneumostome. Respiratory behaviour can be operantly conditioned
by applying a mechanical stimulus to the open pneumostome whenever the animal
attempts to breathe. This aversive reinforcement to the open pneumostome
results in its immediate closure and a significant reduction in the overall
aerial respiratory activity (Lukowiak et
al., 1996).
Although operant conditioning has been studied before in invertebrates, little or no effort has been made to explore the effects of different contingency patterns on the ability to learn in these model systems. Three questions are addressed in the present paper. (i) Is PR is sufficient to induce learning and a subsequent memory similar to that produced by a CR procedure? (ii) Once the acquisition of learning and its consolidation into memory using a CR procedure has occurred, can a PR procedure extend memory persistence? (iii) Finally, in snails subjected to a CR/PR training procedure, will the behaviour be more resistant to extinction (i.e. PREE), as has been demonstrated in various vertebrate preparations for over 60 years? The present findings serve as a basis for future experiments in which the neuronal mechanisms that occur under partial reinforcement in comparison with continuous reinforcement may be elucidated.
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Materials and methods |
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Training and testing procedures
Apparatus and the general operant training procedure
A 11 beaker filled with 500 ml of eumoxic water was made hypoxic by
bubbling N2 through it for 20 min. The individually marked snails
were placed into the hypoxic water for a 10 min period of acclimation. During
this period, they were free to open and close their pneumostome. At the end of
this period, all snails were gently pushed under the water, and the training
then began.
The reinforcing stimulus used in these experiments was a tactile stimulus to the pneumostome area applied as the pneumostome began to open. The tactile stimulus resulted in closure of the pneumostome; the snails usually remained at the water's surface. The tactile stimulus used throughout these experiments did not elicit the whole-body withdrawal/escape response. The time of each stimulus was recorded.
Experiment 1
Continuous reinforcement (CR). Snails were subjected to three 30
min training sessions with each training session separated by 1 h. A 30 min
memory test session was administered the following day to test for long-term
memory. Every pneumostome opening was immediately followed by a tactile
stimulus to the pneumostome area, resulting in immediate closure of the
pneumostome.
Partial reinforcement (PR). Snails were subjected to three 30 min training sessions separated by 1 h. Snails receiving PR were given reinforcement on every second opening (50 % of openings were reinforced) and fell into two categories: those receiving reinforcement every odd-numbered opening (i.e. reinforced on the first, third, fifth pneumostome opening, etc.) and those receiving reinforcement every even-numbered opening (i.e. reinforced on the second, fourth, sixth pneumostome opening, etc.). The time of each pneumostome opening was recorded.
Experiment 2
CR only. Snails received two 45 min training sessions separated by
1 h. A 45 min memory test session was administered either 2 or 3 days later.
Again, every pneumostome opening was immediately followed by a tactile
stimulus to the pneumostome area, resulting in immediate closure of the
pneumostome. The time of each stimulus was recorded.
CR followed by PR. Snails received two 45 min training sessions separated by 1 h on day 1 in which every pneumostome opening resulted in reinforcement (i.e. the CR schedule). On day 2, they received two further 45 min training sessions separated by 1 h. However, these snails now received reinforcement on every odd-numbered pneumostome opening (i.e. the PR schedule). Three days later (day 5), a 45 min memory test was given. During the memory test, all openings were reinforced (i.e. the CR schedule).
PR followed by CR. Snails first received two 45 min PR training sessions separated by 1 h on day 1. On day 2, they received a further two 45 min CR training sessions separated by 1 h. Three days later (day 5), a 45 min memory test was given. During the memory test, all openings were reinforced (i.e. the CR schedule).
Experiment 3
CR followed by PR and extinction training. Snails initially
received two 45 min CR training sessions separated by 1 h on day 1. On day 2,
they received a further two 45 min PR training sessions separated by 1 h. On
day 3, they received two 45 min extinction training sessions separated by 1 h.
In the extinction training sessions, no reinforcement stimuli were
administered. That is, animals were allowed to open their pneumostome without
receiving any reinforcement. The following day (day 4), a 45 min memory test
was given. During the memory test, all openings were reinforced (i.e. the CR
schedule).
PR followed by CR and extinction training. Snails first received two 45 min PR training sessions separated by 1 h on day 1. On day 2, they received two 45 min CR training sessions separated by 1 h. On day 3, they received two 45 min extinction training sessions separated by 1 h. The following day (day 4), a 45 min memory test was given. During the memory test, all openings were reinforced (i.e. the CR schedule).
Operational definitions of learning, memory and extinction
We have operationally defined learning and memory as we have previously
done (Lukowiak et al., 1996,
2000
;
Spencer et al., 1999
).
Briefly, associative learning is defined as a significant effect of training
on the number of attempted pneumostome openings (one-way analysis of variance,
ANOVA, P<0.05; followed by a post-hoc Fisher's LSD
protected t-test, P<0.05 within each separate group). The
number of attempted pneumostome openings in the final training session had to
be significantly less than the number of attempted pneumostome openings in the
first session.
Memory was defined as being present if: (i) the number of attempted pneumostome openings in the memory test session was not significantly different from the number of attempted openings in the last training session and (ii) the number of attempted openings in the memory test session was significantly less than the number of attempted openings in the first training session.
Extinction was defined as being present if the number of attempted pneumostome openings in the memory test session was significantly greater than the number of attempted openings in the last training session.
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Results |
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Next, we wished to examine whether the PR schedule before or after the CR schedule differentially influenced learning and/or the duration of memory retention. To perform these experiments, we used a slightly different CR training procedure to produce learning and long-term memory. We used two naive groups of snails (N=20 and N=19) to show that two 45 min CR training sessions separated by a 1 h interval result in learning and long-term memory that persists for 2 days but not for 3 days (Fig. 2). We then turned our attention to the effect that a combined PR/CR schedule had on the ability of snails to learn and form memory using the two 45 min training session procedure. Thus, one group of snails (the CR/PR group, Fig. 3A) was given two 45 min CR training sessions with an interval of 1 h between each training session on day 1 and two 45 min PR training sessions of on day 2. A second group (the PR/CR group, Fig. 3B) of snails received the PR training sessions on day 1 and the CR training sessions on day 2. In the CR/PR group, the snails exhibited learning and long-term memory when tested 3 days after the final PR training session (i.e. on day 5). That is, the number of attempted pneumostome openings in the memory test session was not significantly different from the number in session 4 (the last training session) but was significantly different from that in session 1 (P<0.01) (Fig. 3A). In the PR/CR group, there was learning, but long-term memory was not demonstrated 3 days later. That is, the number of attempted pneumostome openings on the second CR training session (session 4) was statistically smaller than the number of attempted openings in the first CR training session (session 3). However, the number of attempted openings in the memory test session was significantly greater than the number in the last CR training session (session 4) but was not different from the number in the first CR training session (session 3) (Fig. 3B). Two main conclusions can be drawn from these data. The first is that the order in which snails receive CR and PR training alters their ability to form long-term memory. The second conclusion is that partial reinforcement occurring after the acquisition of learning prolongs the persistence of memory.
|
|
Previously, we have demonstrated that this associatively learned behaviour
can be extinguished (McComb et al.,
2001). We now wished to explore whether the different
reinforcement schedules (CR versus PR) used above affected the
process of extinction. We therefore subjected two different groups of snails
to CR/PR or PR/CR reinforcement schedules prior to administering extinction
training (see Materials and methods). As in the experiments shown in Figs
2 and
3, each group of animals
received two 45 min training sessions separated by a 1 h interval of either CR
or PR on day 1. On day 2, they again received two further 45 min training
sessions separated by a 1 h interval (if they received CR on day 1, they
received PR on day 2 and vice-versa). On day 3, both groups (CR/PR
and PR/CR) received two 45 min extinction training sessions, with each
training session separated by a 1 h rest interval. Twentyfour hours later, we
tested for extinction in both groups. If extinction had occurred, we would
expect there to be no memory. That is, the number of attempted pneumostome
openings observed in the extinction test session should be significantly
greater than the number on the last operant conditioning training session. The
CR/PR group showed no evidence of extinction
(Fig. 4). That is, memory was
still observed [i.e. the extinction test session was not significantly
different from session 4 (the last training session) but was significantly
different from the first CR training session (session 1)]. In contrast, memory
was not found in the PR/CR group, showing that extinction had occurred. That
is, following the extinction training sessions, the number of attempted
pneumostome openings in the extinction test session was significantly
different from that in the last operant training session (session 4).
|
Previously, we have demonstrated that yoked control snails do not exhibit
learning or long-term memory. Although we performed yoked control experiments
on all CR procedures used here, the results have not been presented because
they are similar to those published previously (see
Lukowiak et al., 2000;
Haney and Lukowiak, 2001
).
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Discussion |
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A number of hypotheses have been developed to explain why learning does not
occur with a PR schedule. However, none of them adequately explains why
learning was not observed. For instance, Williams' invariance hypothesis
(Williams, 1989) suggests that
the reduced rate of acquisition with PR training may be due to a decrease in
the number of reinforcement stimuli delivered. That is, using a PR schedule,
the snails receive fewer tactile stimuli in each training session than occurs
with the CR schedule. Fewer reinforcement trials would, in this scenario, lead
to poorer or no learning. As appealing and intuitive as this hypothesis is,
our data are not totally consistent with it. Both associative learning and
longterm memory occur with 15 min training sessions
(Lukowiak et al., 2000
; Smyth
and Lukowiak, 2001). In those two studies, snails received approximately the
same number of tactile stimuli as the snails did in the present study with the
PR schedule. It may be that with a longer PR training session, such as a 1 h
session, learning could be observed. A single 1 h CR session is sufficient to
produce learning and long-term memory that persists for at least 1 day
(Lukowiak et al., 2000
). Such
experiments are planned in the future.
In addition to the snails' inability to form a learned association with the
50 % PR schedule, we showed that this PR training procedure has a number of
significant effects on subsequent memory formation. The first of these effects
was the detrimental (i.e. decreased length of memory persistence) effect on
the ability to form memory following subsequent CR training sessions
(Fig. 3B). That is, even though
there was no significant change in the number of tactile stimuli delivered
over the two PR training sessions, these `PR-challenged' snails could not form
memories as long-lasting as could naïve snails with subsequent CR
training (Fig. 3). This result
could be interpreted as a form of `blocking', which has previously been seen
in both vertebrate and molluscan preparations
(Sahley et al., 1981). It is
not understood why this blocking effect occurs at a mechanistic level.
However, the effect is not due to the fact that there were two PR sessions
together with two CR sessions. When the two CR sessions occurred first,
long-term memory was still observed (in fact, it existed for longer; see
below) following the PR sessions (compare
Fig. 2B with
Fig. 3A). Thus, the order of CR
versus PR sessions is of obvious importance. One advantage of our
model system over most other systems is that we may be able to determine at
the level of a single neuron, RPeD1, known to be necessary for aerial
respiratory behaviour, what the cellular changes are that accompany PR/CR or
CR/PR training.
The second effect on memory formation of PR training was an increase in the
persistence of long-term memory when PR training occurred after learning had
occurred with CR training. Two 45 min CR training sessions result in a memory
that persists for 2 but not for 3 days
(Fig. 2). However, we found
that if, following the two CR training sessions, snails received two 45 min PR
sessions, long-term memory persisted for at least 3 days
(Fig. 3A). That is, long-term
memory was extended by at least 1 day. Again, this demonstrates that the
presentation order of PR and CR has significantly different effects. The order
of CR/PR presentation can thus either increase or decrease memory persistence.
These data parallel the differences in memory persistence that occur when
`massed' versus `spaced' training are compared. While the same level
of performance is achieved (i.e. learning) with massed versus spaced
training, spaced training normally produces a much longer-lasting memory
(Lukowiak et al., 1998). CR
reinforcement at the beginning of the acquisition phase of learning appears to
be necessary but, once some threshold has been reached, a PR schedule can be
implemented to maintain the acquired response
(Hothersall, 1966
).
A third effect of PR on memory retention was the finding that, following
the CR/PR training sequence, memory was resistant to extinction
(Fig. 4). Previously, we have
demonstrated that the associatively learned decrease in aerial respiration can
be extinguished (McComb et al.,
2001). Using similar extinction protocols we found that, following
the CR/PR training sequence, extinction was not observed. That is, memory was
still present. This has been termed the partial reinforcement extinction
effect (PREE) (Skinner, 1938
;
Humphreys, 1939
).
Experimenters have noted this phenomenon in learning studies involving
vertebrates ranging from toads (Muzio et
al., 1994
) to humans
(Svartdal, 2000
;
Leonard, 1975
). To our
knowledge, this is the first time that PREE has been demonstrated for operant
conditioning in a mollusc.
We still do not understand why the PR schedule of reinforcement following
learning acquisition results in a more persistent memory. Amsel's `frustration
theory' (Mackintosh, 1974)
proposes that non-reinforced conditioning, as occurs with PR, leads to an
internal state called frustration. Frustration ultimately leads to increased
attention, thus allowing for stronger associations between the behaviour and
the reinforcing stimuli. This would explain why a PR schedule after
acquisition with a CR schedule might lead to a longer-lasting memory or one
more resistant to extinction. However, in the context of our experiments, it
is uncertain how the absence of a `poke to the pneumostome' would lead to
`frustration' in the snails. A second hypothesis is termed the
PearceHall model (Bouton and Sunsay,
2001
). In this scenario, the intermixture of reinforced and
unreinforced trials increases the `attention' of the subject. Attention is
increased because the trial outcomes are always `surprising'. As stated above,
increased attention should increase association strength and thus allow memory
to be more persistent. Whether any of these hypotheses is adequate to explain
the underlying neuronal mechanisms of learning and retention of memory will be
studied in our model system.
Although the PREE has been well documented at the behavioural level, few
studies have been performed to determine its underlying neuronal mechanisms.
Evidence from lesion studies in vertebrates points to the hippocampus as the
site responsible. Thus, the PREE is prevented if lesions are made in mammals
before training to the hippocampus
(Gonzalez et al., 2000;
Jarrard et al., 1986
) or to
the dorsal ascending noradrenergic bundle, which projects to the hippocampus
(Owen et al., 1982
). Moreover,
lesions to the medial pallium, the amphibian homologue of the hippocampus,
also prevent the PREE (Muzio et al.,
1994
). The discovery of the PREE in Lymnaea stagnalis
offers the opportunity to explore this effect at the level of single neurons
known to be both necessary and sufficient for aerial respiratory behaviour
(Syed et al., 1990
,
1992
;
Spencer et al., 1999
).
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Acknowledgments |
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