Temporal distortions pervade our daily experience and are well evidenced in laboratory studies. Numerous variables have the capacity to distort the perceived duration of events. For example, duration is subjectively lengthened by visual flickers (e.g., Ortega & López, 2008
), click-trains (e.g., Penton-Voak et al., 1996
) and negative emotional arousal (e.g., Grommet et al., 2011
). In contrast, duration is subjectively shortened by positive stimuli (e.g., Ogden et al., 2015
) and shameful facial expressions (e.g., Gil & Droit-volet, 2011
). Pain, in particular, has shown the most distorting effects on time perception (e.g., Rey et al., 2017
Numerous studies show that pain distorts perceptions of time. For example, in a temporal bisection task, which involved categorising a series of comparison durations as more similar to a previously learnt short or long duration, participants gave longer temporal judgments in trials that included the presentation of an electric shock (Fayolle, Gil, & Droit-Volet, 2015
). The effect of pain on perceived duration has a magnitude that is typically greater than that observed for negatively valenced visual and auditory stimuli (Gil & Droit-Volet, 2011
; Ogden, Moore, et al., 2014
; Ogden, Wearden, & Montgomery, 2014
). Furthermore, the extent of temporal distortions due to a painful stimulus increases with pain intensity (Piovesan et al., 2019
The distortions to time evoked by pain experience are often understood within the framework of Scalar Expectancy Theory (SET, Gibbon, Church, & Meck, 1984
). SET proposes that time perception and timed behaviour are accomplished by three distinct processes. The raw representation of time is encoded by a pacemaker accumulator clock. According to SET, at the start of a to-be-timed event, output from the pacemaker is transferred to the accumulator via the closure of the switch. The amount of accumulated output forms the representation of duration, with a greater level of accumulation indicating longer duration. This information is then transferred to short term memory (STM), for use in single trials, and reference memory, which is part of the long-term memory (Cassel & Pereira de Vasconcelos, 2015
), for use over longer periods of time or multiple trial. The contents of STM and reference memory are then compared by some decision threshold to enable behavioural output.
Within the SET framework, temporal distortions caused by pain are usually explained by a change in the rate at which the internal clock emits output (Fayolle et al., 2015
). This change is thought to occur, because pain experience increases physiological arousal, which in turn increases the output rate of the putative clock (see Piovesan et al., 2019
; Ogden, Henderson, et al., 2019
; Ogden, MacKenzie-Phelan, et al., 2019
for discussion). However, while there is good evidence for pain altering internal clock speed, it is unclear whether pain influences the operation of other component processes of SET, for example the memorization of duration. This is in part, because research has focused on examining the effect of pain on the immediate perception of duration in which memory load is low. No research, to date, has tested how pain may influence the retention of duration information in long-term reference memory over a period of delay.
There are two potential ways in which pain may affect the memorization of duration information. (1) Pain may disrupt encoding to, retention in and retrieval from reference memory, leading to an impairment in memory for duration. (2) Pain may enhance encoding to, retention in and retrieval from reference memory, improving memory for duration. These possibilities are discussed below.
Pain may be expected to impair memory for duration, because it affects the general cognitive processes upon which temporal processing is reliant (Buhle & Wager, 2010
; Eccleston & Crombez, 1999
). Accurate temporal processing requires sufficient attention, working memory and executive function (Brown, 2006
; Ogden, Moore, et al., 2014
; Ogden, Wearden, et al., 2014
; Zélanti & Droit-Volet, 2011
). When these resources are exceeded or impaired timing is disrupted, becoming more variable and less accurate (Brown, 1997
; Ogden et al., 2011
), possibly because (1) representations of duration in reference memory are themselves more variable, or because (2) they are more difficult to retrieve from reference memory when working memory and executive resources are limited (Ogden et al., 2014
; Ogden, Wearden, et al., 2014
Indeed, a study showed that nurses who were asked to memorise a 4-s duration and to recall it after 24 h, provided less accurate and more variable responses if they were exposed to high levels of stress during the 24-h delay, perhaps due to reduced attentional resources (Cocenas-Silva, Droit-Volet, & Gherardi-Donato, 2019
). It is also well established that pain impairs the maintenance of items in memory (Dick & Rashiq, 2007
) and recognition accuracy (Forkmann et al., 2016
). Pain also impairs attentional processing (Moore, Keogh, & Eccleston, 2012
; Van Damme, Crombez, & Lorenz, 2007
) and executive function (Moriarty, McGuire, & Finn, 2011
). Leavitt and Katz (2006
) suggested that pain affects memory processes, possibly because pain functions as a distractor leading to reduced attentive resources dedicated to the experimental task. It is, therefore, possible that pain may impair the attentional, memory and executive resources required to encode and maintain duration representations in memory, leading to impaired future recall of duration.
Conversely, however, it is possible that pain may enhance the accuracy of memory for duration. In general cognition, memories for emotional events are often superior to those for neutral events (Brown & Kulik, 1977
; Kensinger & Corkin, 2003
; Lindström & Bohlin, 2011
). Temporal memories also appear to be enhanced by emotions. Cocenas-Silva Bueno, and Droit-Volet (2012
) used a temporal generalisation task to examine how memory for the perceived duration of emotional and neutral events was affected by a delay between encoding and recall. While perceived duration of neutral stimuli was subjectively longer after a 24-h delay than after immediate encoding, the perceived duration of emotional stimuli was not distorted following the 24-h delay. Furthermore, variability of temporal judgments after the 24-h delay was greater for neutral stimuli than for emotional stimuli. The improvement of emotions on memory for duration was found to also persist after 6 months delay between training and testing (Rattat & Droit-Volet, 2007
). Like other forms of memory, memory for duration, therefore, appears to be less vulnerable to distortion and decay when emotional than when neutral.
Emotions may enhance memory for duration, because emotions promote the release of the adrenal stress hormones that facilitate memory consolidation by the hippocampus (LaBar & Cabeza, 2006
; McGaugh, 2000
). This results in arousing emotions enhancing memory for events (D’Argembeau & Van der Linden, 2004
; Dunbar & Lishman, 1984
; Sharot & Phelps, 2004
). Similar to emotion, pain also is a highly arousing experience and promotes the release of adrenal stress hormones (Bear, Connors, & Paradiso, 2007
) and, therefore, may also be expected to enhance memory for duration.
Establishing the way in which pain influences memory for duration is important if we are to develop a complete picture of the way in which emotional somatosensory stimuli distort time. The current study, therefore, sought to establish how durations stored in reference memory were influenced by the experience of pain during the encoding of duration information.
The current study tested the effect of experiencing low pain (Experiment 1) and high pain (Experiment 2) during the encoding of a non-painful temporal stimulus on immediate and delayed temporal generalisation performance. In each experiment, participants completed four temporal generalisation tasks. Each task was split into two phases, a learning phase and a testing phase. In the learning phase, the participants’ task was to memorize the duration of a tone (standard duration), while they experienced either (1) painful stimulation on their arm or (2) neutral stimulation on their arm. In the testing phase, the participants’ task was to indicate whether a series of comparison durations were the same duration as that presented in the learning phase. The testing phase either occurred immediately after the learning phase or following a 15-min delay. A 15-min delay was selected on the basis of previous research indicating that this is sufficient for memory consolidation to take place (Lechner, Squire, & Byrne, 1999
) and on the basis of temporal studies demonstrating significant memory deterioration following a 15-min delay (e.g., Lieving et al., 2006
; Wearden & Ferrara, 1993
; Wearden, Parry, & Stamp, 2002
). No additional (i.e., painful or neutral) stimulation was experienced during the testing phase. All participants, therefore, completed four versions of this task (i) no-pain immediate testing, (ii) no-pain delayed testing, (iii) pain immediate testing and (iv) pain delayed testing.
It was expected that the 15-min delay would decrease temporal accuracy and temporal discrimination in the no-pain condition, confirming previous studies (e.g., Lieving et al., 2006
; Wearden & Ferrara, 1993
; Wearden et al., 2002
). Second, two potential outcomes were hypothesised for the effect of pain on immediate and delayed testing. Learning a duration in a state of pain could either impair
memory processing, leading to poorer recognition of the learnt duration and more variable, less accurate responding in comparison with learning the duration in a neutral state. Alternatively, learning a duration in a state of pain could enhance
memory processing of the duration, leading to better identification of the learnt duration and less variable, more accurate responding in comparison with learning the duration in a neutral state.
The current study sought to establish the effect of low pain (Experiment 1) and high pain (Experiment 2) on the memorization of duration. Participants completed temporal generalisation tasks in which they encoded a standard duration while experiencing concurrent neutral or painful somatosensory stimulation. Participants then completed a recognition task in which they identified the standard duration from an array of comparison durations, in the absence of pain, either immediately after encoding or after a 15-min delay.
For both low and high pain intensities, when testing occurred immediately after the encoding of the standard duration, there were no consistent and systematic effects of pain on responses. There were no significant differences in response accuracy, response variability and FWHM between the immediate testing pain and no pain conditions. Although peak time was significantly higher in the low pain than no pain condition (Experiment 1), and there was a significantly greater proportion of YES responses to the longest comparison in the pain than no-pain condition (Experiment 1), there were no differences in responses for the other comparison durations. Furthermore, these findings were not replicated when a higher intensity pain stimulus was used (Experiment 2). This suggests that experiencing pain during stimulus encoding did not systematically affect the immediate recognition of temporal information. This supports Cocenas-Silva et al.'s (2012
) findings, which showed that emotion did systematically not affect the temporal generalisation performance in a temporal generalisation task when the testing phase occurred immediately after the learning phase.
Comparison of the pain and no-pain delayed testing conditions showed a similar pattern of results. For participants exposed to low pain, peak time was higher in the pain delay than in the no-pain delay condition. However, there was no significant difference in the mean proportion of YES responses, response accuracy, response variability and response spread across the two conditions. For participants exposed to high pain, there was no significant difference in the mean proportion of YES responses, peak time, accuracy or response spread. Together these findings suggest that low and high pain do not have consistent and systematic effects on memory for duration. This contrasts with Cocenas-Silva et al. (2019
) which showed that high stress levels were associated with more variable and less accurate temporal responses in a 24-h delayed temporal generalisation task. It also contrasts with Cocenas-Silva et al. (2012
) which showed that memory for duration of emotional events is less vulnerable to distortion and decay than memory for duration of neutral events.
Collectively, the findings of Experiments 1 and 2 suggest that experiencing pain during the encoding of a temporal stimulus does not have a systematic effect on immediate or delayed recognition of this temporal stimulus. This finding contrasts with expectations that pain during encoding may impair future recognition due to distraction and disruption to cognition, or, enhance future recognition because of a pain-induced increase in the neurochemicals associated with consolidation in the hippocampus.
One possible explanation for the null effect of pain observed in the current study is that the delay imposed between learning and testing was not sufficient to reveal the effect of pain. While there is some evidence to suggest that memory consolidation can occur in a relatively short period of time, for example, within 12 min of encoding (Lechner et al., 1999
), there is also evidence to suggest that consolidation takes significantly longer and is aided by sleep (see Walker et al., 2003
; Stickgold, 2005
for discussion). Indeed, benefits of consolidation periods of longer than 1 h have been demonstrated specifically for duration (Cocenas-Silva et al., 2014
) and previous studies demonstrating effects of emotion on memory for duration have sometimes imposed longer delays between learning and testing. For example, Cocenas-Silva et al. (2012
) imposed a 24-h delay between learning and testing. It is, therefore, possible that a longer retention period would elicit an effect of pain on memory for duration. However, it should be noted that significant effects of short delays comparable to those used in this study have been reported in other studies. For example, a 10-s delay between learning and testing phases in temporal generalisation tasks has been found to impair temporal performance (e.g., Lieving et al., 2006
; Wearden & Ferrara, 1993
; Wearden et al., 2002
). Future research should, however, consider the effect of longer delays when examining the effect of pain experience on duration stored in reference memory.
Another possibility is that the pain administered during this study did not affect memory for duration, because the pain was not itself task-relevant. Piovesan et al. (2019
) demonstrated that task-relevancy determines pain distortions to perceived time during verbal estimation tasks; clear lengthening effects of pain on perceived duration were only observed when the to-be-timed stimulus was itself painful. Concurrent pain, which was not timed, did not distort perceived duration of a neutral to-be-timed stimulus. Similar observations have been made in studies examining the timing of non-painful emotional stimuli (Ogden et al., 2015
Although task relevance offers an explanation as to why the standards encoded during pain were not remembered as systematically longer than the standards encoded during neutral somatosensory stimulation, it does not explain why pain did not disrupt the cognitive processes upon which memory consolidation are reliant. Pain akin to that administered in this study has been shown to impair attention (Moore et al., 2012
; Van Damme et al., 2007
), executive function (Moriarty et al., 2011
), working memory (Dick & Rashiq, 2007
) and recognition memory (Leavitt & Katz, 2006
). Therefore, despite task irrelevant pain not disrupting the timing process itself, there is good evidence to suggest that it should have disrupted the memorization process, leading to poorer recognition performance.
This raises the possibility that duration is somehow “protected” from the disruptive effects of pain on memory. At present, it is unclear why this would be. One possibility is that in the same way in which emotional distortions to time are thought to have an adaptive origin (see Droit-Volet & Gil, 2009
; Lake, LaBar, & Meck, 2016
; Piovesan et al., 2019
for discussion), there may be an adaptive origin to duration information encoded during pain or injury being protected from disruption. Indeed, although pain has a substantial affective component, pain is often not classified as an emotion per se, but is considered a complex biopsychosocial construct, where physiological, social, affective and cognitive dimensions all interact to create the experience of pain (Engel, 1980
). The multifaceted nature of pain experience may, therefore, contribute towards it preventing disruption to distortion to temporal information. Future research should, therefore, examine more broadly the effects of pain on memory for duration.
A final possibility is that the length of the durations used minimised the effect of pain on their memorization. In the current study, the standard durations were all less than 1 s long. Short, sub-second durations are thought to be processed by different neural circuits to longer multiple second intervals (see Lewis & Miall, 2003a
for discussion). Most notably, while the timing of short epochs is thought to place relatively little demand on sustained attentional processing, the timing of longer multi-second or multi-minute epochs requires significantly greater sustained attentional processing (Lewis & Miall, 2003a
). Pain experience disrupts sustained attentional processing (see Eccleston & Crombez, 1999
) and it is, therefore, possible that pain may have a greater effect on the memorization of longer durations due to the effect of pain on the sustained attentional resources required to process these epochs. Future research should, therefore, explore the effect of pain on longer duration ranges.