Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T18:22:54.324Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain and personality bases of insensitivity to infant cues in neglectful mothers: An event-related potential study

Published online by Cambridge University Press:  24 January 2011

María José Rodrigo ,
Inmaculada León ,
Ileana Quiñones ,
Agustín Lage ,
Sonia Byrne  and
María Antonieta Bobes
María José Rodrigo*
Affiliation:
University of La Laguna
Inmaculada León
Affiliation:
University of La Laguna
Ileana Quiñones
Affiliation:
Cuban Neuroscience Center
Agustín Lage
Affiliation:
Cuban Neuroscience Center
Sonia Byrne
Affiliation:
University of La Laguna
María Antonieta Bobes
Affiliation:
Cuban Neuroscience Center
*
Address correspondence and reprint requests to: María José Rodrigo, Facultad de Psicología, Campus de Guajara, Universidad de La Laguna, Tenerife, Spain; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

This investigation examined the neural and personality correlates of processing infant facial expressions in mothers with substantiated neglect of a child under 5 years old. Event-related potentials (ERPs) were recorded from 14 neglectful and 14 control mothers as they viewed and categorized pictures of infant cries, laughs, and neutral faces. Maternal self-reports of anhedonia and empathy were also completed. Early (negative occipitotemporal component peaking at around 170 ms on the scalp [N170] and positive electrical potential peaking at about 200 ms [P200]) and late positive potential (LPP) components were selected. Both groups of mothers showed behavioral discrimination between the different facial expressions via reaction time and accuracy measures. Neglectful mothers did not exhibit increased N170 amplitude at temporal leads in response to viewing crying versus laughing and neutral expressions compared to control mothers. Both groups had greater P200 and LPP amplitudes at centroparietal leads in response to viewing crying versus neutral facial expressions. However, neglectful mothers displayed an overall attenuated brain response in LPP that was related to their higher scores in social anhedonia but not to their empathy scores. The ERP data suggest that the brain's failures in the early differentiation of cry stimuli and in the sustained processing of infant expressions related to social anhedonia may underlie the insensitive responding in neglectful mothers. The implications of these results for the design and evaluation of preventive interventions are discussed.

Type
Regular Articles
Information
Development and Psychopathology , Volume 23 , Issue 1 , February 2011 , pp. 163 - 176
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnfred, S. M., & Chen, A. C. N. (2004). Exploration of somatosensory P50 gating in schizophrenia spectrum patients: Reduced P50 amplitude correlates to social anhedonia. Psychiatry Research, 125, 147–160.CrossRefGoogle ScholarPubMed
Ashley, V., Vuilleumier, P., & Swick, D. (2004). Time course and specificity of event-related potentials to emotional expressions. NeuroReport, 19, 211–216.CrossRefGoogle Scholar
Azizian, A., & Polich, J. (2007). Evidence for attentional gradient in the serial position memory curve from ERPs. Journal of Cognitive Neuroscience, 19, 2071–2081.CrossRefGoogle Scholar
Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., & Juffer, F. (2003). Less is more: Meta-analyses of sensitivity and attachment interventions in early childhood. Psychological Bulletin, 129, 195–215.CrossRefGoogle ScholarPubMed
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 42, 241–251.CrossRefGoogle ScholarPubMed
Batty, M., & Taylor, M. J. (2003). Early processing of the six basic facial emotional expressions. Cognitive Brain Research, 17, 613–620.CrossRefGoogle ScholarPubMed
Bentin, A., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience, 8, 551–565.CrossRefGoogle ScholarPubMed
Bobes, M. A., Martin, M., Olivares, E., & Valdes-Sosa, M. (2000). Different scalp topography of brain potentials related to expression and identity matching of faces. Cognitive Brain Research, 9, 249–260.CrossRefGoogle ScholarPubMed
Bousha, D. M., & Twentyman, C. T. (1984). Mother–child interaction style in abuse, neglect and control groups: Naturalistic observations in the home. Journal of Abnormal Child Psychology, 93, 106–114.CrossRefGoogle ScholarPubMed
Bradley, M. M., Codispoti, M., Cuthbert, B. N., & Lang, P. J. (2001). Emotion and motivation: I. Defensive and appetitive reactions in picture processing. Emotion, 1, 276–299.CrossRefGoogle ScholarPubMed
Brown, L. H., Silvia, P. J., Myin-Germeys, I., & Kwapil, T. R. (2007). When the need to belong goes wrong: The expression of social anhedonia and social anxiety in daily life. Psychological Science, 18, 778–782.CrossRefGoogle ScholarPubMed
Bruder, G. E., Tenke, C. E., Towey, J. P., Leite, P., Fong, R., Stewart, J. E., et al. (1998). Brain ERPs of depressed patients to complex tones in an oddball task: Relation of reduced P3 asymmetry to physical anhedonia. Psychophysiology, 35, 54–63.CrossRefGoogle Scholar
Cacciopo, J. T., & Berntson, G. G. (1999). The affect system: Architecture and operating characteristics. Current Directions in Psychological Science, 8, 133–137.CrossRefGoogle Scholar
Carmel, D., & Bentin, S. (2002). Domain specificity versus expertise: Factors influencing distinct processing of faces. Cognition, 83, 1–29.CrossRefGoogle ScholarPubMed
Carretié, L., Mercado, M., Tapia, J. A., & Hinojosa, J. A. (2001). Emotion, attention, and the “negativity bias,” studied through event-related potentials. International Journal of Psychophysiology, 41, 75–85.CrossRefGoogle ScholarPubMed
Chapman, L. J., & Chapman, J. P. (1978). The Revised Physical Anhedonia Scale. Unpublished manuscript. University of Wisconsin, Madison.Google Scholar
Chapman, L. J., Chapman, J. P., Kwapil, T. R., Eckblad, M., & Zinser, M. C. (1994). Putatively psychosis-prone subjects 10 years later. Journal of Abnormal Psychology, 103, 171–183.CrossRefGoogle ScholarPubMed
Christensen, M. J., Brayden, R. M., Dietrich, M. S., McLaughlin, F. J., Sherrod, K. B., & Altemeier, W. A. (1994). The prospective assessment of self-concept in neglectful and physically abusive low income mothers. Child Abuse & Neglect, 18, 225–232.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Curtis, W. J. (2005). An event-related potential study of the processing of affective facial expressions in young children who experienced maltreatment during the first year of life. Development and Psychopathology, 17, 641–677.CrossRefGoogle ScholarPubMed
Codispoti, M., Ferrari, V., & Bradley, M. M. (2007). Repetition and event-related potentials: Distinguishing early and late process in affective picture perception. Journal of Cognitive Neuroscience, 19, 577–586.CrossRefGoogle ScholarPubMed
Crittenden, P., Lang, C., Claussen, A. H., & Partridge, M. F. (2000). Relations among mothers' procedural, semantic, and episodic internal representational models of parenting. In Crittenden, P. M. & Claussen, A. H. (Eds.), The organization of attachment relationships: Maturation, culture, and context (pp. 214–233). New York: Cambridge University Press.Google Scholar
Cuthbert, B. N., Schupp, H. T., Bradley, M. M., Birbaumer, N., & Lang, P. J. (2000). Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biological Psychology, 52, 95–111.CrossRefGoogle ScholarPubMed
Davis, M. (1980). A multidimensional approach to individual differences in empathy. Catalogue of Selected Documents in Psychology, 10, 85.Google Scholar
Davis, M. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44, 113–126.CrossRefGoogle Scholar
Dawson, G., Webb, S. J., Wijsman, E., Schellenberg, G., Estes, A., Munson, J., et al. (2005). Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: Implications for a model of abnormal development of social brain circuitry in autism. Development and Psychopathology, 17, 679–697.CrossRefGoogle Scholar
Delphanque, S., Lavoie, M., Silvert, L., & Sequeira, H. (2004). Modulation of cognitive processing by emotional valence studied through event-related potentials in humans. Neuroscience Letters, 356, 1–4.CrossRefGoogle Scholar
Dennis, T., & Chen, C. (2007). Emotional face processing and attention performance in three domains: Neurophysiological mechanisms and moderating effects of trait anxiety. International Journal of Psychophysiology, 65, 10–19.CrossRefGoogle ScholarPubMed
Donovan, W. L., Leavitt, L. A., & Walsh, R. O. (1997). Cognitive set and coping strategy affect mothers' sensitivity to infant cries: A signal detection approach. Child Development, 68, 760–772.CrossRefGoogle ScholarPubMed
Dubowitz, H., Pitts, S. C., Litrownik, A. J., Coxd, C. E., Runyan, D., & Black, M. M. (2005). Defining child neglect based on child protective services data. Child Abuse & Neglect, 29, 493–511.CrossRefGoogle ScholarPubMed
Eckblad, M., Chapman, L. J., Chapman, J. P., & Mishlove, M. (1982). The Revised Social Anhedonia Scale. Unpublished manuscript, University of Wisconsin, Madison.Google Scholar
Egeland, B., & Erickson, M. F. (1987). Psychologically unavailable caregiving: The effects on development of young children and the implications for intervention. In Brassard, M., Germain, B., & Hart, S. (Eds.), Psychological maltreatment of children and youth (pp. 110–120). New York: Pergamon Press.Google Scholar
Eimer, M. (2000). Event-related brain potentials distinguish processing stages involved in face perception and recognition. Clinical Neurophysiology, 111, 694–705.CrossRefGoogle ScholarPubMed
Eimer, M., & Holmes, A. (2002). An ERP study on the time course of emotional face processing. NeuroReport, 13, 427–431.CrossRefGoogle Scholar
Eimer, M., Holmes, A., & Mglone, F. P. (2003). The role of spatial attention in the processing of facial expression: An ERP study of rapid brain responses to six basic emotions. Cognitive, Affective & Behavioral Neuroscience, 3, 7–110.CrossRefGoogle ScholarPubMed
Erickson, M. F., & Egeland, B. (2002). Child neglect. In Myers, J. B., Berliner, L., Briere, J., Hendrix, C. T., Jenny, C., & Reid, T. A. (Eds.), The APSAC handbook on child maltreatment (2nd ed., pp. 3–20). Thousand Oaks, CA: Sage.Google Scholar
Facchinetti, L. D., Imbiriba, L. A., Azevedo, T. M., Vargas, C. D., & Volchan, E. (2006). Postural modulation induced by pictures depicting prosocial or dangerous contexts. Neuroscience Letters, 410, 52–56.CrossRefGoogle ScholarPubMed
Franken, I. H. A., Van Strien, J. W., & Nijs, U. M. T. (2006). Effect of hedonic tone on event-related potential measures of cognitive processing. Psychiatry Research, 142, 233–239.CrossRefGoogle ScholarPubMed
Freedman, L. R., Rock, D., Roberts, S. A., Cornblatt, B. A., & Erlenmeyer-Kimiling, L. (1998). The New York high-risk project: Attention, anhedonia and social outcome. Schizophrenia Research, 30, 1–9.CrossRefGoogle ScholarPubMed
Friedrich, W. N., Tyler, J. D., & Clark, J. (1985). Personality and psychophysiological variables in abusive, neglectful and low-income control mothers. Journal of Nervous and Mental Disease, 173, 449–460.CrossRefGoogle ScholarPubMed
Frody, A. M., & Lamb, M. E. (1980). Child abusers' responses to infant smiles and cries. Child Development, 51, 238–241.CrossRefGoogle Scholar
Gard, D. E., Kring, A. M., Gard, M. G., Horan, W. P., & Green, M. F. (2007). Anhedonia in schizophrenia: Distinctions between anticipatory and consummatory pleasure. Schizophrenia Research, 93, 253–260.CrossRefGoogle ScholarPubMed
Gaudin, J. M. (1999). Child neglect: Short-term and long-term outcomes. In Dubowitz, H. (Ed.), Neglected children: Research, practice and policy (pp. 89–108). Thousand Oaks, CA: Sage.CrossRefGoogle Scholar
Gaudin, J. M., Polansky, N. A., Kilpatrick, A. C., & Shilton, P. (1996). Family functioning in neglectful families. Child Abuse & Neglect, 20, 363–377.CrossRefGoogle ScholarPubMed
Hoffman, M. L. (1984). Interaction of affect and cognition in empathy. In Izard, C. E. & Kagan, R. B. (Eds.), Emotions, cognition, and behavior (pp. 103–131). Cambridge: Cambridge University Press.Google Scholar
Holmes, A., Vuilleumier, P., & Eimer, M. (2003). The processing of emotional facial expression is gated by spatial attention: Evidence from event-related brain potentials. Cognitive Brain Research, 16, 174–184.CrossRefGoogle ScholarPubMed
Howell, D. C. (1987). Satistical methods for psychology. Boston: PWS–Kent.Google Scholar
Huang, Y., & Luo, Y. (2006). Temporal course of emotional negativity bias: An ERP study. Neuroscience Letters, 398, 91–96.CrossRefGoogle ScholarPubMed
Kerem, E., Fishman, N., & Josselson, R. (2001). The experience of empathy in everyday relationships: Cognitive and affective elements. Journal of Social and Personal Relationships, 18, 709–729.CrossRefGoogle Scholar
Keselman, H. J., & Rogan, J. (1980). Repeated measures F test and psychophysiological research: Controlling the number of false positives. Psychophysiology, 17, 499–503.CrossRefGoogle Scholar
Krolak-Salmon, P., Fischer, C., Vighetto, A., & Mauguiére, F. (2001). Processing of facial emotional expression: Spatio-temporal data as assessed by scalp event-related potentials. European Journal of Neuroscience, 13, 987–994.CrossRefGoogle ScholarPubMed
Lang, P., Bradley, M. M., & Cuthbert, B. N. (1997). Motivated attention: Affect, activation, and action. In Lang, P., Simons, R. F., & Balaban, M. (Eds.), Attention and orienting: Sensory and motivational processes (pp. 97–126). Hillsdale, NJ: Erlbaum.Google Scholar
Leppänen, J. M., Moulson, M. C., Vogel-Farley, V. K., & Nelson, C. A. (2007). An ERP study of emotional face processing in the adult and infant brain. Child Development, 78, 232–245.CrossRefGoogle ScholarPubMed
Marinkovic, K., & Halgren, E. (1998). Human brain potentials related to the emotional expression, repetition, and gender of faces. Psychobiology, 26, 348–356.CrossRefGoogle Scholar
Mathalon, D. H., Ford, J. M., Rosenbloom, M., & Pfefferbaum, A. (2000). P300 reduction and prolongation with illness duration in schizophrenia. Biological Psychiatry, 47, 413–427.CrossRefGoogle ScholarPubMed
Miller, G. A., Simons, R. F., & Lang, P. J. (1984). Electrocortical measures of information processing deficit in anhedonia. Annals of the New York Academy of Sciences, 425, 598–602.CrossRefGoogle ScholarPubMed
Mishlove, M., & Chapman, L. J. (1985). Social anhedonia in the prediction of psychosis proneness. Journal of Abnormal Psychology, 94, 384–396.CrossRefGoogle ScholarPubMed
Miyoshi, M., Katayama, J., & Morotomi, T. (2004). Face-specific N170 component is modulated by facial expressional change. NeuroReport, 15, 911–914.CrossRefGoogle ScholarPubMed
Oster, H., Hegely, D., & Nagel, L. (1992). Adult judgments and fine-grained analysis of infant facial expressions: Testing the validity of a priori coding formulas. Developmental Psychology, 28, 1115–1131.CrossRefGoogle Scholar
Parker, S. W., Nelson, C. A., & BEIP Core Group. (2005). The impact of early institutional rearing on the ability to discriminate facial expressions of emotion: An event-related potential study. Child Development, 76, 1–19.CrossRefGoogle ScholarPubMed
Pérez-Albéniz, A., De Paúl, J., Etxeberría, J., Montes, M. P., & Torres, E. (2003). Adaptación del Interpersonal Reactivity Index (IRI) al español. Psicothema, 15, 267–272.Google Scholar
Picton, T. W., Lins, O. G., & Sherg, M. (1995). The recording and analysis of event-related potentials. In Boller, F. & Grafman, J. (Eds), Handbook of Neuropsychology (Vol. 10, pp. 3–73). Amsterdam: Elsevier.Google Scholar
Pizzagalli, D. A., Lehman, D., Hendrick, A. M., Regard, M., Pascual-Marqui, R. D., & Davidson, R. (2002). Affective judgments of faces modulate early activity (~160 ms) within the fusiform gyri. NeuroImage, 16, 663–677.CrossRefGoogle ScholarPubMed
Pollak, S. D., Cicchetti, D., Hornung, K., & Reed, A. (2000). Recognizing emotion in faces: Developmental effects of child abuse and neglect. Developmental Psychology, 36, 679–688.CrossRefGoogle ScholarPubMed
Porges, S. W. (2003). Social engagement and attachment. A phylogenetic perspective. Annals of the New York Academy of Science, 1008, 31–47.CrossRefGoogle ScholarPubMed
Ritter, W., & Ruchkin, D. S. (1992). A review of event-related potential components discovered in the context of studying P3. Annals of the New York Academy of Sciences, 658, 1–32.CrossRefGoogle ScholarPubMed
Rodrigo, M. J., Correa, A. D., Máiquez, M. L., Martín, J. C., & Rodríguez, G. (2006). Family preservation services in Canary Islands: Predictors of the efficacy of a Parenting program for families at risk of social exclusion. European Psychologist, 11, 57–70.CrossRefGoogle Scholar
Rodriguez, G., Rodrigo, M. J., Janssens, J., & Triana, B. (in press). Maternal conceptions of the parenting role and mother–child collaborative behaviors in at-risk contexts. European Journal of Developmental Psychology.Google Scholar
Röschke, J., & Wagner, P. (2003). A confirmatory study on the mechanisms behind reduced P300 waves in depression. Neuropsychopharmacology, 28, 9–12.CrossRefGoogle Scholar
Schumacher, J. A., Slep, A. M. S., & Heyman, R. E. (2001). Risk factors for child neglect. Aggression and Violent Behavior, 6, 231–254.CrossRefGoogle Scholar
Schupp, H. T., Junghöfer, M., Weike, A. I., & Hamm, A. O. (2004). The selective processing of briefly presented affective pictures: An ERP analysis. Psychophysiology, 41, 441–449.CrossRefGoogle ScholarPubMed
Schupp, H. T., Öhman, A., Junghöfer, M., Weike, A. I., Stockburger, J., & Hamm, A. O. (2004). The facilitated processing of threatening faces: An ERP analysis. Emotion, 4, 189–200.CrossRefGoogle ScholarPubMed
Seifritz, E., Esposito, F., Neuhoff, J. G., Luthi, A., Mustovic, H., Dammann, G., et al. (2003). Differential sex-independent amygdale response to infant crying and laughing in parents versus non-parents. Biological Psychiatry, 54, 1367–1375.CrossRefGoogle Scholar
Shahar, G. (2001). Maternal personality and distress as predictors of child neglect. Journal of Research in Personality, 35, 537–545.CrossRefGoogle Scholar
Shipman, K., Edwards, A., Brown, A., Swisher, L., & Jennings, E. (2005). Managing emotion in a maltreating context: A pilot study examining child neglect. Child Abuse & Neglect, 29, 1015–1029.CrossRefGoogle Scholar
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007). Brain basis of early parent–infant interactions: Psychology, physiology, and in vivo functional neuroimaging studies. Journal of Child Psychology and Psychiatry, 48, 262–287.CrossRefGoogle ScholarPubMed
Termine, N. T., & Izard, C. E. (1988). Infants' responses to their mothers' expressions of joy and sadness. Developmental Psychology, 24, 223–229.CrossRefGoogle Scholar
Vuilleumier, P., & Pourtois, G. (2007). Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia, 45, 174–194.CrossRefGoogle ScholarPubMed
Wismer Fries, A. B., & Pollak, S. D. (2004). Emotion understanding in postinstitutionalized Eastern European children. Development and Psychopathology, 16, 355–369.Google Scholar