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Unraveling the Electrophysiological Activity Behind Recognition Memory

An Exploratory Event Related Potential (ERP) Study

Published Online:https://doi.org/10.1027/0269-8803/a000263

Abstract. Traditionally, most event related potential (ERP) studies of memory retrieval have been reported during item-recognition tasks. Those studies lead to two well-known ERP memory components termed FN400 (familiarity) and LPC (recollection). Nevertheless, some critics have raised concerns regarding the actual meaning of that activity since it emerges as the result of contrasting two different memory traces (previously studied vs. seen for the first time), and it is registered after the target presentation. Therefore, they possibly depict operations not related to memory itself but some cognitive processes associated with recognition memory. Based on those critics, we propose an innovative approach to study electrophysiological activity underlying recognition memory. We compared two very similar tasks with only one of them requiring subjects to actively retrieve a “cue-target” pair of visual stimuli from memory, while the other task required subjects to recognize the target stimulus as equal/different to the cue. Because of this experimental manipulation, we assured that active memory retrieval processes take place between the presentation of the cue and the target stimuli for only one of the tasks. As a result, responses upon the targets can give us valuable information regarding ERP components associated with recognition based on memory retrieval. We found three components possibly related to brain computations necessary to achieve correct target recognition. A N200-like component linked to executive functions (inhibition) from frontal cortices, a P300-like component, related to the expectation of the target stimulus, and a P600-like component associated to recognition based on LTM retrieval. These results help us to understand the complexity behind ERP components associated with recognition memory.

References

  • Andreau, J. M., & Torres Batán, S. (2019). Exploring lateralization during memory through hemispheric pre-activation: Differences based on the stimulus type. Laterality Asymmetries of Body, Brain and Cognition, 24, 393–416. https://doi.org/10.1080/1357650X.2018.1531422 First citation in articleCrossrefGoogle Scholar

  • Andreau, J. M., Torres Batán, S., & Iorio, A. A. (2019). The time course of associative memory retrieval for pictorial stimulus. An exploratory event-related potential study. Psychology & Neuroscience, 13, 32–50. https://doi.org/10.1037/pne0000186 First citation in articleCrossrefGoogle Scholar

  • Baddeley, A. (1998). Recent developments in working memory. Current Opinion in Neurobiology, 8, 234–238. https://doi.org/10.1016/s0959-4388(98)80145-1 First citation in articleCrossrefGoogle Scholar

  • Cabeza, R. (1999). Functional neuroimaging of episodic memory retrieval. In E. TulvingEd., Memory, consciousness, and the brain: The Tallinn conference (pp. 76–90). Philadelphia, PA: The Psychology Press. First citation in articleGoogle Scholar

  • Cabeza, R., Kapur, S., Craik, F. I., McIntosh, A. R., Houle, S., & Tulving, E. (1997). Functional neuroanatomy of recall and recognition: A PET study of episodic memory. Journal of Cognitive Neuroscience, 9, 254–265. https://doi.org/10.1162/jocn.1997.9.2.254 First citation in articleCrossrefGoogle Scholar

  • Coulson, S., King, J., & Kutas, M. (1998). Expect the unexpected: Event-related brain response to morphosyntactic violations. Language and Cognitive Processes, 13, 21–58. https://doi.org/10.1080/016909698386582 First citation in articleCrossrefGoogle Scholar

  • Curran, T., Tepe, K. L., & Piatt, C. (2006). ERP explorations of dual processes in recognition memory. In H. D. ZimmerA. MecklingerU. LindenbergerEds., Binding in human memory: A neurocognitive approach (pp. 467–492). Oxford, UK: Oxford University Press. First citation in articleGoogle Scholar

  • Donchin, E. (1981). Presidential Address, 1980: Surprise!…Surprise? Psychophysiology, 18, 493–513. https://doi.org/10.1111/j.1469-8986.1981.tb01815.x First citation in articleCrossrefGoogle Scholar

  • Folstein, J. R., & Van Petten, C. (2008). Influence of cognitive control and mismatch on the N2 component of the ERP: A review. Psychophysiology, 45, 152–170. https://doi.org/10.1111/j.1469-8986.2007.00602.x First citation in articleCrossrefGoogle Scholar

  • Friederici, A. D., Von Cramon, D. Y., & Kotz, S. A. (1999). Language related brain potentials in patients with cortical and subcortical left hemisphere lesions. Brain, 122, 1033–1047. https://doi.org/10.1093/brain/122.6.1033 First citation in articleCrossrefGoogle Scholar

  • Funahashi, S., & Andreau, J. M. (2013). Prefrontal cortex and neural mechanisms of executive function. Journal of Physiology-Paris, 107, 471–482. https://doi.org/10.1016/j.jphysparis.2013.05.001 First citation in articleCrossrefGoogle Scholar

  • García-Larrea, L., & Cézanne-Bert, G. (1998). P3, positive slow wave and working memory load: A study on the functional correlates of slow wave activity. Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section, 108, 260–273. https://doi.org/10.1016/S0168-5597(97)00085-3 First citation in articleCrossrefGoogle Scholar

  • Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage, 15, 870–878. https://doi.org/10.1006/nimg.2001.1037 First citation in articleCrossrefGoogle Scholar

  • Gouvea, A. C., Phillips, C., Kazanina, N., & Poeppel, D. (2010). The linguistic processes underlying the P600. Language and Cognitive Processes, 25, 149–188. https://doi.org/10.1080/01690960902965951 First citation in articleCrossrefGoogle Scholar

  • Greve, A., van Rossum, M. C. W., & Donaldson, D. I. (2007). Investigating the functional interaction between semantic and episodic memory: Convergent behavioral and electrophysiological evidence for the role of familiarity. NeuroImage, 34, 801–814. https://doi.org/10.1016/j.neuroimage.2006.07.043 First citation in articleCrossrefGoogle Scholar

  • Guillem, F., N’Kaoua, B., Rougier, A., & Claverie, B. (1995). Intracranial topography of event‐related potentials (N400/P600) elicited during a continuous recognition memory task. Psychophysiology, 32, 382–392. https://doi.org/10.1111/j.1469-8986.1995.tb01221.x First citation in articleCrossrefGoogle Scholar

  • Guillem, F., Rougier, A., & Claverie, B. (1999). Short-and long-delay intracranial ERP repetition effects dissociate memory systems in the human brain. Journal of Cognitive Neuroscience, 11, 437–458. https://doi.org/10.1162/089892999563526 First citation in articleCrossrefGoogle Scholar

  • Henson, R. N., Hornberger, M., & Rugg, M. D. (2005). Further dissociating the processes involved in recognition memory: An FMRI study. Journal of Cognitive Neuroscience, 17(7), 1058–1073. https://doi.org/10.1162/0898929054475208 First citation in articleCrossrefGoogle Scholar

  • Henson, R. N. A., Shallice, T., & Dolan, R. J. (1999). Right prefrontal cortex and episodic memory retrieval: A functional MRI test of the monitoring hypothesis. Brain, 122, 1367–1381. https://doi.org/10.1093/brain/122.7.1367 First citation in articleCrossrefGoogle Scholar

  • Kotchoubey, B. (2005). Event-related potential measures of consciousness: Two equations with three unknowns. Progress in Brain Research, 150, 427–444. https://doi.org/10.1016/S0079-6123(05)50030-X First citation in articleCrossrefGoogle Scholar

  • Lavric, A., Pizzagalli, D. A., & Forstmeier, S. (2004). When “go” and “nogo” are equally frequent: ERP components and cortical tomography. European Journal of Neuroscience, 20, 2483–2488. https://doi.org/10.1111/j.1460-9568.2004.03683.x First citation in articleCrossrefGoogle Scholar

  • Miyashita, Y., Higuchi, S. I., Sakai, K., & Masui, N. (1991). Generation of fractal patterns for probing the visual memory. Neuroscience Research, 12, 307–311. https://doi.org/10.1016/0168-0102(91)90121-e First citation in articleCrossrefGoogle Scholar

  • Mognon, A., Jovicich, J., Bruzzone, L., & Buiatti, M. (2011). ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. Psychophysiology, 48, 229–240. https://doi.org/10.1111/j.1469-8986.2010.01061.x First citation in articleCrossrefGoogle Scholar

  • Münte, T. F., Szentkuti, A., Wieringa, B. M., Matzke, M., & Johannes, S. (1997). Human brain potentials to reading syntactic errors in sentences of different complexity. Neuroscience Letters, 235, 105–108. https://doi.org/10.1016/s0304-3940(97)00719-2 First citation in articleCrossrefGoogle Scholar

  • Orme, E., Brown, L. A., & Riby, L. M. (2017). Retrieval and monitoring processes during visual working memory: An ERP study of the benefit of visual semantics. Frontiers in Psychology, 8, 1080. https://doi.org/10.3389/fpsyg.2017.01080 First citation in articleCrossrefGoogle Scholar

  • Papageorgiou, C., Liappas, I., Asvestas, P., Vasios, C., Matsopoulos, G. K., Nikolaou, C., … Rabavilas, A. (2001). Abnormal P600 in heroin addicts with prolonged abstinence elicited during a working memory test. Neuroreport, 12, 1773–1778. https://doi.org/10.1097/00001756-200106130-00051 First citation in articleCrossrefGoogle Scholar

  • Parker, A.Bussey, T. J.Wilding, E. L. (Eds.). (2005). The cognitive neuroscience of memory: Encoding and retrieval (Vol. 1), London, UK: Psychology Press. First citation in articleCrossrefGoogle Scholar

  • Pergola, G., Trotta, M., & Suchan, B. (2013). Asymmetric hemispheric contribution to ERPs in associative memory indexes goal relevance and quantity of information. Behavioural Brain Research, 241, 7–16. https://doi.org/10.1016/j.bbr.2012.11.041 First citation in articleCrossrefGoogle Scholar

  • Polich, J. (2003). Overview of P3a and P3b. In J. PolichEd., Detection of change: Event-related potential and fMRI findings (pp. 83–98). Boston, MA: Kluwer Academic Press. First citation in articleGoogle Scholar

  • Polich, J. (2007). Updating P300: An integrative theory of P3a and P3b. Clinical Neurophysiology, 118, 2128–2148. https://doi.org/10.1016/j.clinph.2007.04.019 First citation in articleCrossrefGoogle Scholar

  • Polich, J. (2012). Neuropsychology of P300. In S. J. LuckE. S. KappenmanEds., The Oxford handbook of event-related potential components (pp. 159–188). Oxford, UK: Oxford University Press. First citation in articleGoogle Scholar

  • Pritchard, W. S. (1981). Psychophysiology of P300. Psychological Bulletin, 89, 506. https://doi.org/10.1037/0033-2909.89.3.506 First citation in articleCrossrefGoogle Scholar

  • Rugg, M. D. (1995). Event-related potential studies of human memory. In M. S. GazzanigaEd., The cognitive neurosciences (pp. 789–801). Cambridge, MA: MIT Press. First citation in articleGoogle Scholar

  • Rugg, M. D., Fletcher, P. C., Allan, K., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1998). Neural correlates of memory retrieval during recognition memory and cued recall. NeuroImage, 8, 262–273. https://doi.org/10.1006/nimg.1998.0363 First citation in articleCrossrefGoogle Scholar

  • Rugg, M. D., Mark, R. E., Walla, P., Schloerscheidt, A. M., Birch, C. S., & Allan, K. (1998). Dissociation of the neural correlates of implicit and explicit memory. Nature, 392, 595. https://doi.org/10.1038/33396 First citation in articleCrossrefGoogle Scholar

  • Sanquist, T. F., Rohrbaugh, J. W., Syndulko, K., & Lindsley, D. B. (1980). Electrocortical signs of levels of processing: Perceptual analysis and recognition memory. Psychophysiology, 17, 568–576. https://doi.org/10.1111/j.1469-8986.1980.tb02299.x First citation in articleCrossrefGoogle Scholar

  • Simard, F., & Cadoret, G. (2018). Neural correlates of active controlled retrieval development: An exploratory ERP study. Brain and Cognition, 124, 20–28. https://doi.org/10.1016/j.bandc.2018.04.005 First citation in articleCrossrefGoogle Scholar

  • Tibon, R., & Levy, D. A. (2014). The time course of episodic associative retrieval: Electrophysiological correlates of cued recall of unimodal and crossmodal pair-associate learning. Cognitive, Affective, & Behavioral Neuroscience, 14, 220–235. https://doi.org/10.3758/s13415-013-0199-x First citation in articleCrossrefGoogle Scholar

  • Tulving, E., Kapur, S., Markowitsch, H. J., Craik, F. I., Habib, R., & Houle, S. (1994). Neuroanatomical correlates of retrieval in episodic memory: Auditory sentence recognition. Proceedings of the National Academy of Sciences, 91, 2012–2015. https://doi.org/10.1073/pnas.91.6.2012 First citation in articleCrossrefGoogle Scholar

  • Wagner, A. D., Poldrack, R. A., Eldridge, L. L., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. E. (1998). Material specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport, 9, 3711–3717. https://doi.org/10.1097/00001756-199811160-00026 First citation in articleCrossrefGoogle Scholar

  • Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30 years of research. Journal of Memory and Language, 46, 441–517. https://doi.org/10.1006/jmla.2002.2864 First citation in articleCrossrefGoogle Scholar