Advertisement

Neural Dynamics in the Processing of Personal Objects as an Index of the Brain Representation of the Self

  • Francisco MuñozEmail author
  • Pilar Casado
  • David Hernández-Gutiérrez
  • Laura Jiménez-Ortega
  • Sabela Fondevila
  • Javier Espuny
  • José Sánchez-García
  • Manuel Martín-Loeches
Original Paper
  • 44 Downloads

Abstract

Across time, personal belongings incorporate semantic self-knowledge contributing to the subjective meaning of mineness and preference, whose access is prioritized. Although neuroimaging is starting to explore self-knowledge processes, more research is still necessary to better understand many aspects of these processes. One, the timing of the mechanisms involved, is the main purpose of the present study. Here, we investigate the differential patterns of event-related brain potentials and the underlying dynamic causal connectivity between neural generators to self-related objects ranging in self-relevance, as compared to non-personal-related objects. Personal objects elicited lower N2 and higher P3 components compared to non-personal objects, and those with high relevance showed the lowest N2 and the highest P3 amplitudes. Brain sources connectivity corresponding to N2–P3 ERP complex revealed an early connectivity between posterior cingulate/precuneus and parahippocampal gyrus, common for both types of objects. However, this parietal connectivity was kept in later latencies only for personal objects, also intervening the anterior cingulate as the main driver of information flow to the parietal network. Personal objects showed more extensive connectivity between parietal areas and these with anterior cingulate. These findings provide new evidence of a neural connectivity and its temporal course underlying the interplay of lower-level and higher-level cognitive processes relative to personal objects. Further, the results offer new insights on how superordinate mental representations enable distinctive processing of relevant belongings, starting relatively early in time.

Keywords

Self-relevance Object ownership N2 P3 Cortical Midline Structures Effective source connectivity 

Notes

Acknowledgements

This study has been funded by Grant No. PSI2017-82357-P from MINECO (Spain).

References

  1. Andreasen NC, O’Leary D, Ted D, Stephan A, Karim R, Watkins GL, Ponto LBL, Hichwa RD (1995) II. PET studies of memory: novel versus practiced free recall of word lists. NeuroImage 2:296–305.  https://doi.org/10.1006/nimg.1995.1037 CrossRefPubMedGoogle Scholar
  2. Baccalá L, Takahashi DY, Sameshima K (2006) Computer intensive testing for the influence between time series. In: Schelter B, Winterhalder M, Timmer J (eds) Handbook of time series analysis: recent theoretical developments and applications. Wiley, Weinheim, p 411CrossRefGoogle Scholar
  3. Ball AD, Tasaki LH (1992) The role and measurement of attachment in consumer behavior. J Consum Psychol 1:155–172.  https://doi.org/10.1207/s15327663jcp0102_04 CrossRefGoogle Scholar
  4. Başar E, Schmiedt-Fehr C, Oniz A, Başar-Eroğlu C (2008) Brain oscillations evoked by the face of a loved person. Brain Res 1214:105–115CrossRefGoogle Scholar
  5. Beggan JK (1992) On the social nature of non-social perception: the mere ownership effect. J Pers Soc Psychol 62:229–237.  https://doi.org/10.1037/0022-3514.62.2.229 CrossRefGoogle Scholar
  6. Belk RW (1988) Possessions and the self. J Consum Res 15:139–168.  https://doi.org/10.1086/209154 CrossRefGoogle Scholar
  7. Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129–1159.  https://doi.org/10.1162/neco.1995.7.6.1129 CrossRefPubMedGoogle Scholar
  8. Bruce V, Young AW (1986) Understanding face recognition. Br J Psychol 77:305–327.  https://doi.org/10.1111/j.2044-8295.1986.tb02199.x CrossRefPubMedGoogle Scholar
  9. Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929.  https://doi.org/10.1126/science.1099745 CrossRefPubMedGoogle Scholar
  10. Cabeza R, St Jacques P (2007) Functional neuroimaging of autobiographical memory. Trends Cogn Sci 11:219–227.  https://doi.org/10.1016/j.tics.2007.02.005 CrossRefPubMedGoogle Scholar
  11. Carretié L, Hinojosa JA, Martín-Loeches M, Mercado F, Tapia M (2004) Automatic attention to emotional stimuli: neural correlates. Hum Brain Mapp 22:290–299.  https://doi.org/10.1002/hbm.20037 CrossRefPubMedGoogle Scholar
  12. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583.  https://doi.org/10.1093/brain/awl004 CrossRefPubMedGoogle Scholar
  13. Chaumon M, Bishop DVM, Busch NA (2015) A practical guide to the selection of independent components of the electroencephalogram for artifact correction. J Neurosci Methods 250:47–63.  https://doi.org/10.1016/j.jneumeth.2015.02.025 CrossRefPubMedGoogle Scholar
  14. Chen J, Yuan J, Feng T, Chen A, Gu B, Li H (2011) Temporal features of the degree effect in self-relevance: neural correlates. Biol Psychol 87:290–295.  https://doi.org/10.1016/j.biopsycho.2011.03.012 CrossRefPubMedGoogle Scholar
  15. Cloutier J, Kelley WM, Heatherton TF (2011) The influence of perceptual and knowledge-based familiarity on the neural substrates of face perception. Soc Neurosci 6:63–75.  https://doi.org/10.1080/17470911003693622 CrossRefPubMedGoogle Scholar
  16. Conway MA, Singer JA, Tagini A (2004) The self and autobio- graphical memory: correspondence and coherence. Soc Cogn 22:491–529.  https://doi.org/10.1521/soco.22.5.491.50768 CrossRefGoogle Scholar
  17. Coronel JC, Federmeier KD (2016) The N400 reveals how personal semantics is processed: insights into the nature and organization of self-knowledge. Neuropsychologia 84(C):36–43.  https://doi.org/10.1016/j.neuropsychologia.2016.01.029 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cunningham SJ, Turk DJ, MacDonald LM, Macrae CN (2008) Yours or mine? Ownership and memory. Conscious Cogn 17:312–318.  https://doi.org/10.1016/j.concog.2007.04.003 CrossRefPubMedGoogle Scholar
  19. Delorme A, Makeig SD (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21.  https://doi.org/10.1016/j.jneumeth.2003.10.009 CrossRefGoogle Scholar
  20. Delorme A, Mullen T, Kothe C, Zeynep AA, Nima B-S, Andre V, Scott M (2011) EEGLAB, SIFT, NFT, BCILAB, and ERICA: new tools for advanced EEG processing. Comput Intell Neurosci.  https://doi.org/10.1155/2011/130714 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20:143–149.  https://doi.org/10.1016/j.conb.2010.01.004 CrossRefPubMedGoogle Scholar
  22. Evans N, Blanke O (2013) Shared electrophysiology mechanisms of body ownership and motor imagery. NeuroImage 64:216–228.  https://doi.org/10.1016/j.neuroimage.2012.09.027 CrossRefPubMedGoogle Scholar
  23. Foster BL, Dastjerdi M, Parvizi J (2012) Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing. Proc Natl Acad Sci USA 109:15514–15519.  https://doi.org/10.1073/pnas.1206580109 CrossRefPubMedGoogle Scholar
  24. Gallagher S (2000) Philosophical conceptions of the self: implications for cognitive science. Trends Cogn Sci 4:14–21.  https://doi.org/10.1016/S1364-6613(99)01417-5 CrossRefPubMedGoogle Scholar
  25. Gawronski B, Bodenhausen GV, Becker AP (2007) I like it, because I like myself: associative self-anchoring and post-decisional change of implicit evaluations. J Exp Soc Psychol 43:221–232.  https://doi.org/10.1016/j.jesp.2006.04.001 CrossRefGoogle Scholar
  26. Geweke J (1982) Measurement of linear dependence and feedback between multiple time series. J Am Stat Assoc 77:304–313.  https://doi.org/10.1080/01621459.1982.10477803 CrossRefGoogle Scholar
  27. Gillihan SJ, Farah MJ (2005) Is self special? A critical review of evidence from experimental psychology and cognitive neuroscience. Psychol Bull 131:76–97.  https://doi.org/10.1037/0033-2909.131.1.76 CrossRefPubMedGoogle Scholar
  28. Golubickis M, Falben JK, Cunningham WA, Macrae CN (2018) Exploring the self-ownership effect: separating stimulus and response biases. J Exp Psychol Learn Mem Cogn 44:295–306.  https://doi.org/10.1037/xlm0000455 CrossRefPubMedGoogle Scholar
  29. Granger CW (1969) Investigating causal relations by econometric models and cross-spectral methods. Econ J Econ Soc 37:424–438.  https://doi.org/10.2307/1912791 CrossRefGoogle Scholar
  30. Gray H, Ambady N, Lowenthal W, Deldin P (2004) P3 as an index of attention to self-relevant stimuli. J Exp Soc Psychol 40:216–224.  https://doi.org/10.1016/S0022-1031(03)00092-1 CrossRefGoogle Scholar
  31. Greenwald AG, Banaji MR (1989) The self as a memory system: powerful, but ordinary. J Pers Soc Psychol 57:41–54.  https://doi.org/10.1037/0022-3514.57.1.41 CrossRefGoogle Scholar
  32. Guan LL, Qi MM, Zhang QL, Yang J (2014) The neural basis of self-face recognition after self-concept threat and comparison with important others. Soc Neurosci 9:424–435.  https://doi.org/10.1080/17470919.2014.920417 CrossRefPubMedGoogle Scholar
  33. Höller Y, Kronbichler M, Bergmann J, Crone JS, Ladurner G, Golaszewski S (2011) EEG frequency analysis of responses to the own-name stimulus. Clin Neurophysiol 122:99–106.  https://doi.org/10.1016/j.clinph.2010.05.029 CrossRefPubMedGoogle Scholar
  34. Hyvärinen A (1999) Fast and robust fixed-point algorithms for independent component analysis. IEEE Trans Neural Netw Learn Syst 10:626–634.  https://doi.org/10.1109/72.761722 CrossRefGoogle Scholar
  35. Johnson R (1986) A triarchic model of P3 amplitude. Psychophysiology 23:367–384.  https://doi.org/10.1111/j.1469-8986.1986.tb00649.x CrossRefPubMedGoogle Scholar
  36. Kelley WM, Macrae CN, Wyland CL, Caglar S, Inati S, Heatherton TF (2002) Finding the self? An event-related fMRI study. J Cogn Neurosci 14:785–794.  https://doi.org/10.1162/08989290260138672 CrossRefPubMedGoogle Scholar
  37. Kim K, Johnson MK (2012) Extended self: medial prefrontal activity during transient association of self and objects. Soc Cogn Affect Neurosci 7:199–207.  https://doi.org/10.1093/scan/nsq096 CrossRefPubMedGoogle Scholar
  38. Kim K, Johnson MK (2014) Extended self: spontaneous activation of medial prefrontal cortex by objects that are “mine”. Soc Cogn Affect Neurosci 9:1006–1012.  https://doi.org/10.1093/scan/nst082 CrossRefPubMedGoogle Scholar
  39. Klein SB, Kihlstrom JE (1986) Elaboration, organization, and the self-reference effect in memory. J Exp Psychol Gen 115:26–38.  https://doi.org/10.1037/0096-3445.115.1.26 CrossRefPubMedGoogle Scholar
  40. Klein SB, Loftus J (1988) The nature of self-referent encoding: the contributions of elaborative and organizational processes. J Pers Soc Psychol 55:5–11.  https://doi.org/10.1037/h0090411 CrossRefGoogle Scholar
  41. Klein SB, Chan RL, Loftus J (1999) Independence of episodic and semantic self-knowledge: the case from autism. Soc Cogn 17:413–436.  https://doi.org/10.1521/soco.1999.17.4.413 CrossRefGoogle Scholar
  42. Klein SB, Nichols S (2012) Memory and the sense of personal identity. Mind 121:677–702.  https://doi.org/10.1093/mind/fzs080 CrossRefGoogle Scholar
  43. Klimesch W (2012) Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 16:606–617.  https://doi.org/10.1016/j.tics.2012.10.007 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Knyazev GG (2007) Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci Biobehav Rev 31:377–395.  https://doi.org/10.1016/j.neubiorev.2006.10.004 CrossRefPubMedGoogle Scholar
  45. Knyazev GG (2013) EEG correlates of self-referential processing. Front Hum Neurosci 7:264.  https://doi.org/10.3389/fnhum.2013.00264 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Korzeniewska A, Crainiceanu M, Kus R, Franaszczuk P, Crone N (2008) Dynamics of event-related causality in brain electrical activity. Hum Brain Mapp 29:1170–1192.  https://doi.org/10.1002/hbm.20458 CrossRefPubMedGoogle Scholar
  47. LeBarr AN, Shedden JM (2017) Psychological ownership: the implicit association between self and already-owned versus newly-owned objects. Conscious Cogn 48:190–197.  https://doi.org/10.1016/j.concog.2016.11.012 CrossRefPubMedGoogle Scholar
  48. Legrand D, Ruby P (2009) What is self-specific? Theoretical investigation and critical review of neuroimaging results. Psychol Rev 116:252–282.  https://doi.org/10.1037/a0014172 CrossRefPubMedGoogle Scholar
  49. Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Sackeim HA, Lisanby SH (2004) Parietal cortex and representation of the mental self. Proc Natl Acad Sci USA 101:6827–6832.  https://doi.org/10.1073/pnas.0400049101 CrossRefPubMedGoogle Scholar
  50. Ma Y, Han S (2010) Why we respond faster to the self than to others? An implicit positive association theory of self-advantage during implicit face recognition. J Exp Psychol Hum Percept Perform 36:619–633.  https://doi.org/10.1037/a0015797 CrossRefPubMedGoogle Scholar
  51. Maddock RJ (1999) The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain. Trends Neurosci 22:310–316.  https://doi.org/10.1016/S0166-2236(98)01374-5 CrossRefPubMedGoogle Scholar
  52. Maki RH, McCaul KD (1985) The effects of self-reference versus other reference on the recall of traits and nouns. Bull Psychon Soc 23:169–172.  https://doi.org/10.3758/BF03329817 CrossRefGoogle Scholar
  53. Miyakoshi M, Nomura M, Ohira H (2007) An ERP study on self-relevant object recognition. Brain Cogn 63:182–189.  https://doi.org/10.1016/j.bandc.2006.12.001 CrossRefPubMedGoogle Scholar
  54. Miyakoshi M, Kanayama N, Iidaka T, Ohira H (2010) EEG evidence of face-specific visual self-representation. NeuroImage 50:1666–1675.  https://doi.org/10.1016/j.neuroimage.2010.01.030 CrossRefPubMedGoogle Scholar
  55. Mu Y, Han S (2013) Neural oscillations dissociate between self-related attentional orientation versus evaluation. NeuroImage 67:247–256.  https://doi.org/10.1016/j.neuroimage.2012.11.016 CrossRefPubMedGoogle Scholar
  56. Mullen T (2010) Source Information Flow Toolbox (SIFT) Theoretical Handbook and User Manual. Swartz Center for Computational Neuroscience, San Diego, CAGoogle Scholar
  57. Mullen T R (2014) The dynamic brain: modeling neural dynamics and interactions from human electrophysiological recordings (Order No 3639187). Dissertations & Theses @ University of California; ProQuest Dissertations & Theses A&I. (1619637939)Google Scholar
  58. Neuner I, Arrubla J, Werner CJ, Hitz K, Boers F, Kawohl W, Shah NJ (2014) The default mode network and EEG regional spectral power: a simultaneous fMRI-EEG study. PLoS ONE.  https://doi.org/10.1371/journal.pone.0088214 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Northoff G (2013) Brain and self—a neurophilosophical account. Child Adolesc Psychiatry Ment Health 7:28.  https://doi.org/10.1186/1753-2000-7-28 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Northoff G (2016a) Neurophilosophy and the healthy mind. Learning from the unwell brain. WW Norton & Co, New YorkGoogle Scholar
  61. Northoff G (2016b) Is the self a higher-order or fundamental function of the brain? The “basis model of self-specificity” and its encoding by the brain’s spontaneous activity. Cogn Neurosci 7:203–222.  https://doi.org/10.1080/17588928.2015.1111868 CrossRefPubMedGoogle Scholar
  62. Northoff G, Bermpohl F (2004) Cortical midline structures and the self. Trends Cogn Sci 8:102–107.  https://doi.org/10.1016/j.tics.2004.01.004 CrossRefPubMedGoogle Scholar
  63. Northoff G, Hayes DJ (2011) Is our self nothing but reward? Biol Psychiat 69:1019–1025.  https://doi.org/10.1016/j.biopsych.2010.12.014 CrossRefPubMedGoogle Scholar
  64. Onton J, Westerfield M, Townsend J, Makeig S (2006) Imaging human EEG dynamics using independent component analysis. Neurosci Biobehav Rev 30:808–822.  https://doi.org/10.1016/j.neubiorev.2006.06.007 CrossRefPubMedGoogle Scholar
  65. Paller KA, Ranganath C, Gonsalves B, LaBar KS, Parrish TB, Gitelman DR, Marsel-Mesulam M, Reber PJ (2003) Neural correlates of person recognition. Learn Mem 10:253–260.  https://doi.org/10.1101/lm.57403 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Patel SH, Azzam PN (2005) Characterization of N2 and P3: selected studies of the event-related potential. Int J Med Sci 2:147–154.  https://doi.org/10.7150/ijms.2.147 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Qin P, Northoff G (2011) How is our self-related to midline regions and the default-mode network? NeuroImage 57:1221–1233.  https://doi.org/10.1016/j.neuroimage.2011.05.028 CrossRefPubMedGoogle Scholar
  68. Rogers TB, Kuiper NA, Kirker WS (1977) Self-reference and the encoding of personal information. J Pers Soc Psychol 35:677–688.  https://doi.org/10.1037/0022-3514.35.9.677 CrossRefPubMedGoogle Scholar
  69. Schöne B, Köster M, Gruber T (2018) Coherence in general and personal semantic knowledge: functional differences of the posterior and centro-parietal N400 ERP component. Exp Brain Res 236:2649–2660.  https://doi.org/10.1007/s00221-018-5324-1 CrossRefPubMedGoogle Scholar
  70. Shah NJ, Marshall JC, Zafiris O, Schwab A, Zilles K, Markowitsch HJ, Fink GR (2001) The neural correlates of person familiarity: a functional magnetic resonance imaging study with clinical implications. Brain 124:804–815.  https://doi.org/10.1093/brain/124.4.804 CrossRefPubMedGoogle Scholar
  71. Spreng RN, Mar RA, Kim AS (2009) The common neural basis of autobiographical memory prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. J Cogn Neurosci 21:489–510.  https://doi.org/10.1162/jocn.2008.21029 CrossRefPubMedPubMedCentralGoogle Scholar
  72. St Jacques PL, Kragel PA, Rubin DC (2011) Dynamic neural networks supporting memory retrieval. NeuroImage 57:608–616.  https://doi.org/10.1016/j.neuroimage.2011.04.039 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Strauman TJ, Detloff AM, Sestokas R, Smith DV, Goetz EL, Rivera C, Kwapil L (2013) What shall I be, what must I be: neural correlates of personal goal activation. Front Integr Neurosci 6:1–14.  https://doi.org/10.3389/fnint.2012.00123 CrossRefGoogle Scholar
  74. Su Y, Chen A, Yin H, Qiu J, Lv J, Wei D, Tian F, Tu S, Wang T (2010) Spatiotemporal cortical activation underlying self-referential processing evoked by self-hand. Biol Psychol 85:219–225.  https://doi.org/10.1016/j.biopsycho.2010.07.004 CrossRefPubMedGoogle Scholar
  75. Sugiura M, Shah NJ, Zilles K, Fink GR (2005) Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex. J Cogn Neurosci 17:183–198.  https://doi.org/10.1162/0898929053124956 CrossRefPubMedGoogle Scholar
  76. Sui J, Gu X (2017) Self as object: emerging trends in self research. Trends Neurosci 40:643–653.  https://doi.org/10.1016/j.tins.2017.09.002 CrossRefPubMedGoogle Scholar
  77. Sui J, Humphreys GW (2015) The integrative self: how self-reference integrates perception and memory. Trends Cogn Sci 19:719–728.  https://doi.org/10.1016/j.tics.2015.08.015 CrossRefPubMedGoogle Scholar
  78. Sui J, He X, Humphreys GW (2012) Perceptual effects of social salience: evidence from self-prioritization effects on perceptual matching. J Exp Psychol Hum Percept Perform 38:1105–1117.  https://doi.org/10.1037/a0029792 CrossRefPubMedGoogle Scholar
  79. Sui J, Liu M, Mevorach C, Humphreys GW (2015) The salient self: the left intraparietal sulcus responds to social as well as perceptual-salience after self-association. Cereb Cortex 25:1060–1068.  https://doi.org/10.1093/cercor/bht302 CrossRefPubMedGoogle Scholar
  80. Symons CS, Johnson BT (1997) The self-reference effect in memory: a meta-analysis. Psychol Bull 121:371–394.  https://doi.org/10.1037/0033-2909.121.3.371 CrossRefPubMedGoogle Scholar
  81. Tacikowski P, Nowicka A (2010) Allocation of attention to self-name and self-face: an ERP study. Biol Psychol 84:318–324.  https://doi.org/10.1016/j.biopsycho.2010.03.009 CrossRefPubMedGoogle Scholar
  82. Turk DJ, van Bussel K, Brebner JL, Toma AS, Krigolson O, Handy TC (2011) When “it” becomes “mine”: attentional biases triggered by object ownership. J Cogn Neurosci 23:3725–3733.  https://doi.org/10.1162/jocn_a_00101 CrossRefPubMedGoogle Scholar
  83. Wiener N (1956) The theory of prediction. In: Beckenbach E (ed) Modern mathematics for engineers. McGraw-Hill, New York, pp 165–190Google Scholar
  84. Xu K, Li S, Ren D, Xia R, Xue H, Zhou A, Xu Y (2017) Importance modulates the temporal features of self-referential processing: an event-related potential study. Front Hum Neurosci.  https://doi.org/10.3389/fnhum.2017.00470 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Francisco Muñoz
    • 1
    • 2
    Email author
  • Pilar Casado
    • 1
    • 2
  • David Hernández-Gutiérrez
    • 1
  • Laura Jiménez-Ortega
    • 1
    • 2
  • Sabela Fondevila
    • 1
  • Javier Espuny
    • 1
  • José Sánchez-García
    • 1
  • Manuel Martín-Loeches
    • 1
    • 2
  1. 1.Center for Human Evolution and BehaviorUCM-ISCIIIMadridSpain
  2. 2.Psychobiology & Methods for the Behavioral Sciences DepartmentComplutense University of MadridMadridSpain

Personalised recommendations