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State-dependent memory produced by aerobic exercise
Christopher Miles Elinor Hardman
To cite this Article Hardman, Christopher Miles Elinor(1998) 'State-dependent memory produced by aerobic exercise',
Ergonomics, 41: 1, 20 — 28
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ERGONOMICS , 1998,
VOL.
41,
NO .
1, 20 ± 28
State-dependent memory produced by aerobic exercise
CHRISTOPHER MILES and ELINOR HARDMAN
School of Psychology, University of Wales College of CardiŒ, CardiŒCF1 3YG,
UK
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Keywords: Aerobic exercise; Cue-dependent memory; Recall levels;
State-dependent memory.
In a free recall experiment, participants learned lists of words in two physiological
states: at rest and while exercising aerobically on a bicycle ergometer. Recall of
the words was required in either the state consistent with learning or in the
alternative state. Word lists learned during aerobic exercise were recalled best
during aerobic exercise and vice versa. Greater changes in heart rate in the
changed state conditions were associated with greater retrieval decrements. Recall
levels for words both learned and recalled at exercise were equivalent to those for
words both learned and recalled at rest. This ® nding rules out the possibility that
exercise per se interfered with the original learning. The study is consistent with
the view that state-dependent memory should be viewed as a particular form of
cue-dependent memory.
1. Introduction
The functioning of the human memory system may be characterized as involving the
permanent retention of material with remembering and forgetting conceptualized
respectively as successful recall and a temporary failure to recall. During learning the
participant processes not only the to-be-learned material, but in addition associates
that material with a variety of internal and external contextual cues. The participant
therefore processes a multidimensional complex of stimuli. Forgetting will occur, at
least at the behavioural level, if the contextual cues at test do not su ciently
discriminate between the desired memory and some other competing memories
(Capaldi and Neath 1995). By this account, a change in context necessarily results in
altered stimulus conditions and changing the stimuli present from study to test can
lead to retrieval failure (Tulving 1983). Context can aŒect the accessibility of items
by reducing the eŒectiveness of potential retrieval cues to discriminate between the
target memory and other distracter memories (Eich 1989).
Perhaps the most widely known experiment examining the eŒect on recall of a
context switch between study and test is that reported by Godden and Baddeley
(1975). Experienced scuba divers studied a list of 36 common and unrelated words in
one of two environments: either on land or underwater. Participants later retrieved
the list items either in the original learning environment or in the alternate context.
Even though the location of the dives and time of day were not controlled for, there
was a pronounced context-dependen t retrieval ® nding using free recall: recall
averaged 35% in the consistent learning and retrieval conditions but was markedly
reduced to 24% in the changed conditions. A second experiment required one-half of
the participants to learn a list of words and to recall them on land. The other half
also learned and recalled on land but they were required to enter the pool, swim a
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State-dependen t memory produced by aerobic exercise
21
short distance, dive to a depth of 20 ft, and then return to land prior to recall. Recall
performance of both groups was equivalent, thus ruling out the possibility that
disruption between learning and test was the cause of poorer recall in the ® rst
experiment. A similar context manipulation study with greater ecological validity
(Martin and Aggleton 1993), which used novice divers who were required to learn
and recall decompression tables, has shown an equally powerful context-dependen t
retrieval eŒect.
Each of these studies represents an example of context-dependen t retrieval with
external manipulation of context. However, context may also be manipulated
internally. When context is provided by the pharmacological state of the participant
for instance, the phenomenon is known as state-dependent memory. Such statedependent learning in humans has been demonstrated by Goodwin et al. (1969).
Participants who were given alcohol in training and saline at test performed worse on
a variety of tasks compared to the same state groups. This ® nding does not appear to
be attributabl e to anything speci® c to the drugged state. For example, Weingartner
and Faillace (1971) conducted a state-dependent memory experiment with two
diŒerent groups of participants. One group comprised chronic alcoholics and the
other comprised an equal number of non-alcoholics closely matched to the alcoholic
participants with respect to a variety of demographic variables. Participants were
either intoxicated or sober at list learning and intoxicated or sober at test. Both
groups showed state-dependent memory eŒects. Recall was higher when the test state
matched the learning state in comparison to the changed state condition, thus ruling
out any objection to a separate role of alcohol.
Other state manipulations demonstrating this ® nding include mood congruency
(Bartlett and Santrock 1979) and odour congruency (Schab 1990). In the Bartlett
and Santrock study the mood or aŒective state of participants was altered so that
they were either in a happy or neutral mood at study and a happy or neutral mood at
test. Performance was better for participants in the same-mood conditions. Schab
(1990) ® lled a small room with the odour of chocolate either at study or test or both.
After a 24-h delay performance on a surprise memory test was better when the
odours at learning and test matched. Thus a change in context (whether it be external
or internal) may be conceptualized as in¯ uencing memory performance by removing
or altering potential retrieval cues. For both state- and context-dependen t memory
eŒects the disruption to performance is greatest when the contexts are more
discriminable because of the concomitant change in retrieval cue availability.
Eich (1980) has argued that the ® nding of state-dependent retrieval is determined
to a large extent by the nature of the retrieval task employed. He argues that retrieval
paradigms that provide an explicit cue to the participant with respect to the target
item (e.g. paired associate learning) are not sensitive to state-dependent retrieval
because the probing of memory via an explicit cue provides the participant with a
direct link to the target item in memory. The existence of a direct cue allows the
retrieval process to bypass state-dependent cues that might otherwise be activated
(otherwise known as `the outshining hypothesis’). The deleterious eŒect of changing
state is therefore negated. In those memory paradigms where no explicit retrieval cue
is provided for the participant (e.g. free recall) then the state-dependent retrieval
eŒects are reliable and robust. In this instance, Eich (1980) suggests that `invisible’
cues guide the process of retrieval. The available data therefore force the conclusion
that state-dependent retrieval should be viewed as a cue-dependent phenomenon.
State-dependent retrieval eŒects depend critically on the precise nature of the
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22
C. Miles and E. Hardman
information or cues that are available to the participants at retrieval. If the cues at
test match those at learning then recall is facilitated.
The present study was concerned with extending the ® ndings of state-dependent
retrieval beyond these conditions where internal state is typically manipulated by the
administration of a particular dose of a drug such as alcohol. Participant state was
manipulated by the requirement to pedal a bicycle ergometer at a rate such that heart
rate was elevated to approximately twice the normal resting level. In a repeated
measures design participants’ heart rates were manipulated such that they learned
and retrieved information either at rest or when working at a prede® ned level of
aerobic exercise. Manipulation of heart rate in this way allowed an assessment of the
association between the porportional change in heart rate and the associated change
in recall levels for the changed state combinations.
The present authors employed the same class of memory materials as reported by
Godden and Baddeley (1975) in their study of context-dependen t retrieval. Superior
recall is predicted in those conditions where the heart rate of the participant is
consistent at both learning and retrieval in comparison to the changed state
conditions. In the latter conditions fewer of those state cues present at the original
encoding of the word lists were present at recall. In addition, the extent to which the
porportional change in heart rate between rest and exercise conditions predicted
change in retrieval levels was assessed. In particular, the authors aimed to determine
the extent to which greater changes in heart rate (and therefore retrieval cues) between
learning and retrieval are associated with greater de® cits in retrieval of information.
2. Method
2.1. Participants
Twenty-four undergraduat e participants (6 males and 18 females) from the
University of Wales College of CardiŒtook part in the study. Their age range was
18 ± 22 years with a mean of 20 years 3 months. Each participant received a small
payment.
2.2. Assessment of exercise intensity
This study investigated the eŒect of a change in heart rate between learning and
retrieval on free recall performance. It therefore considered the intensity of exercise
necessary to induce a change in cardiovascular state. Aerobic work commences at a
level of exercise that requires the heart to beat at 60% of an individual’s maximum
heart rate (McArdle et al. 1994). An accepted estimate of maximum heart rate (in
beats per minute, bpm) is `220 Ð the participant’ s age’. Although participants of the
same age will not necessarily have equivalent maximum heart rates, individual
diŒerences should not be of any practical signi® cance in this regard (McArdle et al.
1994). In the current study the participants’ mean age was 20 years 3 months and the
estimated maximum heart rate employed was 200 bpm. Therefore, the minimum
heart rate giving rise to a change in heart rate (as de® ned by aerobic work) is 200
0× 6 = 120 bpm.
To ensure that aerobic work levels were maintained during the exercise
conditions, the points at which anaerobic work starts and aerobic ® nishes required
de® nition. McArdle et al. (1994) describe that point at which maximal aerobic and
minimal anaerobic respiration occurs as the Maximal Aerobic Function (MAF).
MAF is calculated by subtracting chronological age from 180 and adding to this
® gure a ® tness-dependent number (range: Ð 10 to + 5). In the current study, a
´
State-dependen t memory produced by aerobic exercise
23
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minimum level of ® tness was assumed for all participants and an adjustment to MAF
of Ð 10 was therefore employed. Thus, for a participant population with a mean age
of 20 years 3 months a MAF of 150 bpm was employed. The aerobic zone for the
exercise condition was hence calculated as a minimum of 120 bpm and a maximum
of 150 bpm.
2.3. Materials
Four stimulus lists were prepared. Each list comprised 36 trisyllabic words all with
Kucera and Francis (1967) frequency ratings of 1 per million. The lists were spoken
in monotone by a female voice at a rate of 1 word per 2-s and recorded directly on to
an audio tape. Each list was recorded twice with a 10-s interval between lists. The
word lists were presented to the participants over headphones in order to minimize
external noise. At recall, the participants spoke their responses directly into a
microphone that was connected to a second audio cassette recorder. The exercise
condition was undertaken on a Seca bicycle ergometer with an adjustable work load
(resistance) and a meter that provided a visual indication of cadence (pedalling rate).
Each participant wore a Polar Edge heart rate monitor throughout the experiment.
This provides a second-by-second digital record of heart rate.
2.4. Design
A 2-factor repeated measures design was adopted. The ® rst factor refers to learning
condition (exercise versus rest) and the second refers to retrieval condition (exercise
versus rest). Allocation of participants to conditions was counterbalanced such that
each of the 24 participants completed the four experimental combinations in a
diŒerent order. The participants were presented with a diŒerent word list pair at
learning in each experimental combination and each word list pair was used a total
of six times in each of these. Participants attended the laboratory on four consecutive
days at approximately the same time of day and completed a diŒerent experimental
combination on each occasion.
2.5. Procedure
Each participant was tested individually in a soundproofed laboratory. Upon
entering the laboratory the experiment was described to the participants and all were
provided with written task instructions. For all participants the experiment comprised
a 3 min learning phase, a 5 min consolidation phase, and a 2 min retrieval phase. The
participant was made comfortable on the bicycle ergometer and then put on the heart
rate monitor, a pair of headphones and had a microphone positioned as close to the
mouth as possible. During the learning phase of the experiment, participants heard
two presentations of the same to-be-recalled 36-word list 10 s apart. Following
Godden and Baddeley (1975) the second word list was followed by a spoken sequence
of ® ve digits, presented at the rate of one digit per second for immediate recall. This
task was included to limit the extent to which free recall of the lists was a direct
product of subvocal rehearsal strategies. Following this task, there was a 5-min
consolidation interval during which the participant remained on the bicycle
ergometer and was not distracted. There then followed a 2-min free recall period.
The four conditions in which each participant was tested are detailed below.
(1) Rest-Rest(RR): The participant performed the complete task while seated
on, but not pedalling, the bicycle ergometer.
C. Miles and E. Hardman
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24
(2) Rest-Exercise (RE): The participant sat at rest on the bicycle during the list
presentation (learning) phase. During the 5-min (consolidation) interval the
participant remained sitting quietly for the ® rst 3-min. For the remaining 2min, the participant was required to pedal the bicycle at a candence of 60
revolutions per minute (rpm). The resistance of the ergometer was adjusted
such that the participant’s heart rate was elevated to a rate between 120 and
150 bpm. This 2-min period allowed the participant to adapt to the
cardiovascular demands of exercise prior to the retrieval phase. During the 2min retrieval period the participant continued to pedal at the same rate.
(3) Exercise-Rest (ER): Two minutes prior to the learning phase of the
experiment the participant began pedalling at a cadence of 60 rpm. The
resistance of the ergometer was adjusted such that the participant’ s heart rate
was elevated to between 120 and 150 bpm. The participant continued to
pedal at this rate throughout the 2-min learning phase. The participants
rested during the 5-min consolidation phase. The participant then recalled
the words during the 2-min rest period.
(4) Exercise-Exercise(EE): Two minutes prior to the learning phase of the
experiment the participant began pedalling at a cadence of 60 rpm. The
resistance of the ergometer was adjusted such that the participant’ s heart rate
was elevated to between 120 and 150 bpm. The participant continued to
pedal at this rate throughout the learning phase. The participant rested for
the ® rst 3-min of the consolidation phase. For the remaining 2-min the
participant pedalled at the same load and cadence as in the presentation
phase. The participant continued to pedal at the same load and cadence
throughout the 2-min recall phase.
The participant’s heart rate was noted at the beginning and end of each of the
learning, consolidation and retrieval phases of the experiment.
3. Results
3.1. Heart Rate
The mean heart rate associated with all combinations of learning and retrieval is
shown in table 1. A related t-test showed no signi® cant diŒerence (t < 1) between the
mean heart rate data for either the learning and retrieval at rest or learning and
retrieval at exercise combinations.
The heart rate data were converted to a proportional change from resting heart
rate data for each participation prior to analysis, because of individual diŒerences in
cardiovascular e ciency. For each participant the resting heart rate was taken as the
mean heart rate in the learning at rest condition. For every other condition heart rate
Table 1. Mean heart rate (BPM) at learning and retrieval for each of the Rest-Rest (RR);
Rest-Exercise (RE); Exercise-Rest (ER) and Exercise-Exercise (EE) combinations.
Condition
Mean heart
rate (BPM)
Learning
Retrieval
RR
RE
ER
EE
80× 1
80× 0
83× 6
131× 1
134 × 2
85× 5
136 × 3
134 × 1
State-dependen t memory produced by aerobic exercise
25
was calculated as a proportional change from that resting rate. These data were
subjected to a 2-factor (2 2) repeated measures ANOVA with factors participant
state at list learning (exercise versus rest) and participant state at list retrieval
(exercise versus rest). Neither the main eŒect of participant state at learning nor that
of participant state at recall was signi® cant (both Fs < 1) but their interaction was
highly signi® cant (F(1,23)= 247 × 1, p < 0× 001) and the means are shown in table 2.
Further analysis (Newman-Keuls) showed the proportional change in the RE and
ER combinations to be signi® cantly greater (p < 0× 001) in comparison to both the
RR and EE combinations. No other comparisons were signi® cant.
´
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3.2. Correct free recall
The total number of words (max. = 36) recalled by each participant in each
combination was calculated and the data submitted to the same model 2-factor
Table 2. Proportional change in mean heart rate between
learning and retrieval for each of the Rest-Rest (RR);
Rest-Exercise (RE); Exercise-Rest (ER) and ExerciseExercise (EE) combinations.
Condition
RR
0× 008
Figure 1.
RE
0× 6
ER
0× 6
EE
0× 02
Mean number of words recalled for each of the Rest-Rest (RR); Rest-Exercise
(RE); Exercise-Rest (ER) and Exercise-Exercise (EE) combinations.
26
C. Miles and E. Hardman
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ANOVA as described above. Neither the main eŒect of participant state at list
learning nor at list retrieval was signi® cant (both Fs < 1) but their interaction was
highly signi® cant (F(1,23) = 11× 83, p < 0× 005) and is represented in ® gure 1. The
pattern of the interaction is consistent with predictions. Further analysis of the
interaction (Newman-Keuls) showed that both same-state learning-retrieval conditions produced signi® cantly (p < 0× 05) higher levels of recall than either of the
changed-state learning-retrieval conditions.
3.3. False alarms
The data were further analysed to check that the state-dependent eŒect was not a
function of a guessing strategy. There was an examination of the possibility that
participants produced more guess words in the same-state learning retrieval
conditions, which would result in a higher probability of producing a previously
presented word. The same ANOVA model as described above produced no main
eŒects of participant state at either learning or retrieval (both Fs < 1), nor an
interaction between the factors (F < 1).
3.4. Correlation
The extent to which porportional change from the resting heart rate level was
associated with change in recall level for the changing-stat e learning and retrieval
combinations was assessed.
The mean proportional change in heart rate across both changing-stat e
conditions was calculated for each participant (ignoring the sign of the change for
the exercise-rest combination). These scores were correlated (Pearson’s r) with the
average change in recall levels across both changing-stat e conditions (r = 0× 38,
df = 22, p = 0× 06).
4. Discussion
The results of the study demonstrate that a change in cardiovascular activity between
learning and retrieval can exert a powerful state eŒect on retrieval of word lists. The
pattern of data mirrors that shown for shifts in context from above or below water
shown previously (Godden and Baddeley 1975, Martin and Aggleton 1993). On
average the changing state conditions produced a 20% drop in recall performance in
comparison to the same state conditions. It is unlikely that the eŒect of changing
state can be attributed to greater disruption for the changing state combinations
(Strand 1970) during the consolidation phase because the exercise-exercise
combination also required participants to both stop and start pedalling during the
consolidation phase.
In addition, the pattern of the interaction as shown in ® gure 1 demonstrates that the
eŒect of changing state on recall worked in both directions: that is going from rest to
exercise and exercise to rest. Further analysis showed that the state of learning per se
(exercise versus rest) had no in¯ uence on later recall. This ® nding is consistent with the
work of both Tomporowski et al. (1987) who found no impairment in immediate free
recall of 15 word lists for participants on a treadmill working at approximatel y 80%
maximum heart rate and Sjoberg (1980) who showed that exercise on a bicycle
ergometer had no eŒect on paired-associate learning at a range of loadings up to 75%
maximum heart rate. The comparison of rest and exercise conditions is important
because it eliminates the possibility that the interaction was due to either poor encoding
of the stimuli or an inability to retrieve the words while in the exercise condition. The
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State-dependen t memory produced by aerobic exercise
27
data indicate a clear eŒect of changing state on the retrieval of word lists. Material
learned either at rest or while exercising aerobically is better retrieved by participants in
the same as opposed to the alternate state. The environmental context was consistent
across all learning-retrieval combinations and therefore the poorer retrieval in the
changed state conditions may be attributed to a mismatch between the incidental cues
encoded at original presentation of the material and the cues present at retrieval.
The association between the porportional change in heart rate for the changing
state conditions and the number of words retrieved, although only marginally
signi® cant, does suggest that greater changes in cardiovascular activity are associated
with greater reductions in retrieval. This ® nding is consistent with the view that statedependent retrieval is a cue-dependent phenomenon. Those incidental cues
assimilated by the participant at learning become increasingly less eŒective as
retrieval cues as the change in heart rate increases because of the associated increase
in potential distracter cues.
Finally, the act of pedalling the bicycle ergometer will have brought about a
number of changes in physiological state in addition to that of increasing the heart
rate (e.g. rate of oxygen uptake, increase in body temperature). It is likely that a
change in a number of physiological parameters would together have acted to bring
about a change of state in, and therefore associated retrieval cues available to, the
participant. This also applies to the Godden and Baddeley (1975) and the Martin
and Aggleton (1993) studies where the change in context from above and below
water and vice versa was undoubtedly associated with a number of changes in the
physiological state of the participant. The authors measured only change in heart
rate but it is possible that changes in other such physiological parameters may better
predict the performance change. These data may have implications for sports people
who need to memorize information beyond the capacity of their immediate memory
span and who need to recall it while competing. Initial learning of the information
should take place when the physiological state of the competitor most closely
matches that in which recall is required during competition.
Acknowledgements
The authors wish to thank John Aggleton and an anonymous referee for their
comments on an earlier draft of this paper.
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