Abstract
In this study, we sought to examine the effect of experimentally induced somatic pain on memory. Subjects heard a series of words and made categorization decisions in two different conditions. One condition included painful shocks administered just after presentation of some of the words; the other condition involved no shocks. For the condition that included painful stimulations, every other word was followed by a shock, and subjects were informed to expect this pattern. Word lists were repeated three times within each condition in randomized order, with different category judgments but consistent pain-word pairings. After a brief delay, recognition memory was assessed. Non-pain words from the pain condition were less strongly encoded than non-pain words from the completely pain-free condition. Recognition of pain-paired words was not significantly different than either subgroup of non-pain words. An important accompanying finding is that response times to repeated experimental items were slower for non-pain words from the pain condition, compared to non-pain words from the completely pain-free condition. This demonstrates that the effect of pain on memory may generalize to non-pain items experienced in the same experimental context.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andreatta M, Leombruni E, Glotzbach-Schoon E, Pauli P, Muhlberger A (2015) Generalization of contextual fear in humans. Behav Ther 46:583–596. https://doi.org/10.1016/j.beth.2014.12.008
Arndt J, Reder LM (2002) Word frequency and receiver operating characteristic curves in recognition memory: evidence for a dual-process interpretation. J Exp Psychol Learn Mem Cogn 28:830–842
Bauch EM, Rausch VH, Bunzeck N (2014) Pain anticipation recruits the mesolimbic system and differentially modulates subsequent recognition memory. Hum Brain Mapp 35:4594–4606. https://doi.org/10.1002/hbm.22497
Bennion KA, Ford JH, Murray BD, Kensinger EA (2013) Oversimplification in the study of emotional memory. J Int Neuropsychol Soc 19:953–961. https://doi.org/10.1017/S1355617713000945
Berryman C, Stanton TR, Jane Bowering K, Tabor A, McFarlane A, Lorimer Moseley G (2013) Evidence for working memory deficits in chronic pain: a systematic review and meta-analysis. Pain 154:1181–1196. https://doi.org/10.1016/j.pain.2013.03.002
Bingel U, Quante M, Knab R, Bromm B, Weiller C, Buchel C (2002) Subcortical structures involved in pain processing: evidence from single-trial fMRI. Pain 99:313–321
Carlsson K, Andersson J, Petrovic P, Petersson KM, Ohman A, Ingvar M (2006) Predictability modulates the affective and sensory-discriminative neural processing of pain. Neuroimage 32:1804–1814
Castegnetti G, Tzovara A, Staib M, Paulus PC, Hofer N, Bach DR (2016) Modeling fear-conditioned bradycardia in humans. Psychophysiology 53:930–939. https://doi.org/10.1111/psyp.12637
Cave CB, Squire LR (1992) Intact and long-lasting repetition priming in amnesia. J Exp Psychol Learn Mem Cogn 18:509–520
Choi JC, Park SK, Kim YH et al (2006) Different brain activation patterns to pain and pain-related unpleasantness during the menstrual cycle. Anesthesiology 105:120–127
D’Esposito M (2007) From cognitive to neural models of working memory. Philos Trans R Soc Lond B Biol Sci 362:761–772. https://doi.org/10.1098/rstb.2007.2086
Diana RA, Reder LM, Arndt J, Park H (2006) Models of recognition: a review of arguments in favor of a dual-process account. Psychon Bull Rev 13:1–21
Dunsmoor JE, Kroes MC (2019) Episodic memory and Pavlovian conditioning: ships passing in the night. Curr Opin Behav Sci 26:32–39. https://doi.org/10.1016/j.cobeha.2018.09.019
Forkmann K, Wiech K, Ritter C, Sommer T, Rose M, Bingel U (2013) Pain-specific modulation of hippocampal activity and functional connectivity during visual encoding. J Neurosci 33:2571–2581
Forkmann K, Schmidt K, Schultz H, Sommer T, Bingel U (2016) Experimental pain impairs recognition memory irrespective of pain predictability. Eur J Pain 20:977–988. https://doi.org/10.1002/ejp.822
Francis WS (2014) Repetition priming in picture naming: sustained learning through the speeding of multiple processes. Psychon Bull Rev 21:1301–1308. https://doi.org/10.3758/s13423-014-0610-9
Grillon C (2002) Associative learning deficits increase symptoms of anxiety in humans. Biol Psychiatry 51:851–858
Gros DF, Antony MM, Simms LJ, McCabe RE (2007) Psychometric properties of the State-Trait Inventory for Cognitive and Somatic Anxiety (STICSA): comparison to the State-Trait Anxiety Inventory (STAI). Psychol Assess 19:369–381. https://doi.org/10.1037/1040-3590.19.4.369
Henke K (2010) A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 11:523–532. https://doi.org/10.1038/nrn2850
Hood A, Pulvers K, Spady TJ (2013) Timing and gender determine if acute pain impairs working memory performance. J Pain 14:1320–1329. https://doi.org/10.1016/j.jpain.2013.05.015
Keane MM, Cruz ME, Verfaellie M (2015) Attention and implicit memory: priming-induced benefits and costs have distinct attentional requirements. Mem Cognit 43:216–225. https://doi.org/10.3758/s13421-014-0464-4
LaBar KS, Cabeza R (2006) Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7:54–64. https://doi.org/10.1038/nrn1825
LeDoux JE (2014) Coming to terms with fear. Proc Natl Acad Sci USA 111:2871–2878. https://doi.org/10.1073/pnas.1400335111
Leys C, Ley C, Klein O, Bernard P, Licata L (2013) Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J Exp Soc Psychol 49:764–766. https://doi.org/10.1016/j.jesp.2013.03.013
Lonsdorf TB, Menz MM, Andreatta M et al (2017) Don’t fear ‘fear conditioning’: methodological considerations for the design and analysis of studies on human fear acquisition, extinction, and return of fear. Neurosci Biobehav Rev 77:247–285. https://doi.org/10.1016/j.neubiorev.2017.02.026
Lund K, Burgess C (1996) Producing high-dimensional semantic spaces from lexical co-occurrence. Behav Res Methods, Instrum Comput 28:203–208. https://doi.org/10.3758/bf03204766
Mather M, Sutherland MR (2011) Arousal-biased competition in perception and memory. Perspect Psychol Sci 6:114–133. https://doi.org/10.1177/1745691611400234
McCracken LM, Dhingra L (2002) A short version of the Pain Anxiety Symptoms Scale (PASS-20): preliminary development and validity. Pain Res Manag 7:45–50
Migo EM, Mayes AR, Montaldi D (2012) Measuring recollection and familiarity: improving the remember/know procedure. Conscious Cogn 21:1435–1455. https://doi.org/10.1016/j.concog.2012.04.014
Murty VP, Adcock AR (2017) Distinct medial temporal lobe network states as neural contexts for motivated memory formation. In: Hannula DE, Duff MC (eds) The hippocampus from cells to systems: structure, connectivity, and functional contributions to memory and flexible cognition. Springer International Publishing, Cham, pp 467–501
Osman A, Barrios FX, Kopper BA, Hauptmann W, Jones J, O’Neill E (1997) Factor structure, reliability, and validity of the pain catastrophizing scale. J Behav Med 20:589–605
Popov V, Reder LM (2018) Frequency effects on memory: a resource-limited theory. https://osf.io/dsx6y/
Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968–971
Rajaram S (1993) Remembering and knowing: two means of access to the personal past. Mem Cognit 21:89–102
Roelofs J, Peters ML, McCracken L, Vlaeyen JW (2003) The pain vigilance and awareness questionnaire (PVAQ): further psychometric evaluation in fibromyalgia and other chronic pain syndromes. Pain 101:299–306
Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49–53. https://doi.org/10.1038/nature08637
Schreckenberger M, Siessmeier T, Viertmann A et al (2005) The unpleasantness of tonic pain is encoded by the insular cortex. Neurology 64:1175–1183
Schwarze U, Bingel U, Sommer T (2012) Event-related nociceptive arousal enhances memory consolidation for neutral scenes. J Neurosci 32:1481–1487. https://doi.org/10.1523/JNEUROSCI.4497-11.2012
Shields GS, Sazma MA, McCullough AM, Yonelinas AP (2017) The effects of acute stress on episodic memory: a meta-analysis and integrative review. Psychol Bull 143:636–675. https://doi.org/10.1037/bul0000100
Squire LR, Dede AJ (2015) Conscious and unconscious memory systems. Cold Spring Harb Perspect Biol 7:a021667. https://doi.org/10.1101/cshperspect.a021667
Wais PE (2008) FMRI signals associated with memory strength in the medial temporal lobes: a meta-analysis. Neuropsychologia 46:3185–3196. https://doi.org/10.1016/j.neuropsychologia.2008.08.025
Wais PE, Mickes L, Wixted JT (2008) Remember/know judgments probe degrees of recollection. J Cogn Neurosci 20:400–405. https://doi.org/10.1162/jocn.2008.20041
Yonelinas AP, Ritchey M (2015) The slow forgetting of emotional episodic memories: an emotional binding account. Trends Cogn Sci 19:259–267. https://doi.org/10.1016/j.tics.2015.02.009
Yonelinas AP, Aly M, Wang WC, Koen JD (2010) Recollection and familiarity: examining controversial assumptions and new directions. Hippocampus 20:1178–1194. https://doi.org/10.1002/hipo.20864
Zanto TP, Clapp WC, Rubens MT, Karlsson J, Gazzaley A (2016) Expectations of task demands dissociate working memory and long-term memory systems. Cereb Cortex 26:1176–1186. https://doi.org/10.1093/cercor/bhu307
Acknowledgements
This work was supported by a seed grant from the Department of Anesthesiology, University of Pittsburgh, School of Medicine. Further support was provided by a Mentored Research Training Grant (to KMV) from the Foundation for Anesthesia Education and Research (FAER). Salary support for KMV during the initial phase of this project came from an institutional training grant from the National Institutes of Health (T32GM075770). Subject recruitment was assisted by the University of Pittsburgh Clinical Translational Science Institute Research Participant Registry, a project supported by the National Institutes of Health through grant number UL1TR000005. The authors have no relevant financial or other conflicts of interest to disclose related to this work. This work has been improved substantially from its initial form by suggestions from anonymous reviewers, to which the authors are grateful.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vogt, K.M., Norton, C.M., Speer, L.E. et al. Memory for non-painful auditory items is influenced by whether they are experienced in a context involving painful electrical stimulation. Exp Brain Res 237, 1615–1627 (2019). https://doi.org/10.1007/s00221-019-05534-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-019-05534-x