Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T10:57:12.566Z Has data issue: false hasContentIssue false
  • English
  • Français

A developmental increase in allostatic load from ages 3 to 11 years is associated with increased schizotypal personality at age 23 years

Published online by Cambridge University Press:  21 October 2011

Melissa Peskin ,
Adrian Raine ,
Yu Gao ,
Peter H. Venables  and
Sarnoff A. Mednick
Melissa Peskin*
Affiliation:
University of Pennsylvania
Adrian Raine
Affiliation:
University of Pennsylvania
Yu Gao
Affiliation:
University of Pennsylvania
Peter H. Venables
Affiliation:
University of York
Sarnoff A. Mednick
Affiliation:
University of Southern California
*
Address correspondence and reprint requests to: Melissa Peskin, Department of Psychology, University of Pennsylvania, 3720 Walnut Street, Philadelphia, PA 19104-6241; E-mail: peskinf@sas.upenn.edu.
Get access Rights & Permissions [Opens in a new window]

Abstract

Although allostatic load has been investigated in mood and anxiety disorders, no prior study has investigated developmental change in allostatic load as a precursor to schizotypal personality. This study employed a multilevel developmental framework to examine whether the development of increased allostatic load, as indicated by impaired sympathetic nervous system habituation from ages 3 to 11 years, predisposes to schizotypal personality at age 23 years. Electrodermal activity to six aversive tones was recorded in 995 subjects at age 3 years and again at 11 years. Habituation slopes at both ages were used to create groups who showed a developmental increase in habituation (decreased allostatic load), and those who showed a developmental decrease in habituation (increased allostatic load). Children who showed a developmental increase in allostatic load from ages 3 to 11 years had higher levels of schizotypal personality at 23 years. A breakdown of total schizotypy scores demonstrated specificity of findings to cognitive–perceptual features of schizotypy. Findings are the first to document a developmental abnormality in allostasis in relation to adult schizotypal personality. The relative failure to develop normal habituation to repeated stressors throughout childhood is hypothesized to result in an accumulation of allostatic load and consequently increased positive symptom schizotypy in adulthood.

Type
Articles
Information
Development and Psychopathology , Volume 23 , Issue 4: Allostatic Load: Part 2 , November 2011 , pp. 1059 - 1068
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

Allen, P., Freeman, D., & McGuire, P. (2007). Slow habituation of arousal associated with psychosis proneness. Psychological Medicine, 37, 577–582.CrossRefGoogle ScholarPubMed
Bauer, A. M., Quas, J. A., & Boyce, T. W. (2002). Associations between physiological reactivity and children's behavior: Advantages of a multisystem approach. Developmental and Behavioral Pediatrics, 23, 102–113.CrossRefGoogle ScholarPubMed
Bogerts, B. (1997). The temporolimbic system theory of positive schizophrenic symptoms. Schizophrenia Bulletin, 23, 423–435.CrossRefGoogle ScholarPubMed
Buchsbaum, M. S., Nenadic, I., Hazlett, E. A., Spiegel-Cohen, J., Fleischman, M. B., Akhavan, A., et al. (2002). Differential metabolic rates in prefrontal and temporal Brodmann areas in schizophrenia and schizotypal personality disorder. Schizophrenia Research, 54, 141–150.CrossRefGoogle ScholarPubMed
Cadenhead, K. S., Light, G. A., Geyer, M. A., & Braff, D. L. (2000). Sensory gating deficits assessed by the P50 event-related potential in subjects with schizotypal personality disorder. American Journal of Psychiatry, 157, 55–59.CrossRefGoogle ScholarPubMed
Cannon, T. D., Cadenhead, K., Cornblatt, B., Woods, S. W., Addington, J., Walker, E., et al. (2008). Prediction of psychosis in youth at high clinical risk. Archives of General Psychiatry, 65, 28–37.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Curtis, W. J. (Eds.). (2007). A multilevel approach to resilience [Special Issue]. Development and Psychopathology, 19, 627–955.CrossRefGoogle Scholar
Cicchetti, D., & Dawson, G. (Eds.). (2002). Multiple levels of analysis [Special Issue]. Development and Psychopathology, 14, 417–666.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Posner, M. I. (Eds.). (2005). Integrating cognitive and affective neuroscience and developmental psychopathology [Special Issue]. Development and Psychopathology, 17, 569–891.CrossRefGoogle Scholar
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 16–25.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.).Hillsdale, NJ: Erlbaum.Google Scholar
D'Argembeau, A., Collette, F., Van der Linden, M., Laureys, S., Del Fiore, G., Degueldre, C., et al. (2005). Self-referential reflective activity and its relationship with rest: A PET study. NeuroImage, 25, 616–624.CrossRefGoogle Scholar
Dawson, M. E., Filion, D. L., & Schell, A. M. (1989). Is elicitation of the autonomic orienting response associated with allocation of processing resources? Psychophysiology, 26, 560–572.CrossRefGoogle ScholarPubMed
Dawson, M. E., Nuechterlein, K. H., & Liberman, R. P. (1983). Relapse in schizophrenic disorders: Possible contributing factors and implications for behavior therapy. In Rosenbaum, M., Franks, C. M., & Jaffe, Y. (Eds.), Perspectives on behavior therapy in the eighties (pp. 265–286). New York: Springer–Verlag.Google Scholar
Dawson, M. E., Nuechterlein, K. H., Schell, A. M., Gitlin, M., & Ventura, J. (1994). Autonomic abnormalities in schizophrenia: State or trait indicators? Archives of General Psychiatry, 51, 813–824.CrossRefGoogle ScholarPubMed
Dawson, M. E., & Schell, A. M. (2002). What does electrodermal activity tell us about prognosis in the schizophrenia spectrum? Schizophrenia Research, 54, 87–93.CrossRefGoogle ScholarPubMed
Dawson, M. E., Schell, A. M., & Filion, D. L. (2007). The electrodermal system. In Cacioppo, J. T., Tassinary, L. G., & Berntson, G. (Eds.), Handbook of psychophysiology (3rd ed., pp. 159–181). New York: Cambridge University Press.Google Scholar
Dickey, C. C., McCarley, R. W., Voglmaier, M. M., Niznikiewicz, M. A., Seidman, L. J., Hirayasu, Y., et al. (1999). Schizotypal personality disorder and MRI abnormalities of temporal lobe gray matter. Biological Psychiatry, 45, 1393–1402.CrossRefGoogle ScholarPubMed
Dickey, C. C., McCarley, R. W., Xu, M. L., Seidman, L. J., Voglmaier, M. M., Niznikiewicz, M. A., et al. (2007). MRI abnormalities of the hippocampus and cavum septi pellucidi in females with schizotypal personality disorder. Schizophrenia Research 89, 49–58.CrossRefGoogle ScholarPubMed
Epstein, J., Stern, E., & Silbersweig, D. (1999). Mesolimbic activity associated with psychosis in schizophrenia: Symptom-specific P.E.T. studies. In McGinty, J. F. (Ed.), Advancing from the ventral striatum to the extended amygdala: Implications for neuropsychiatry and drug use: In honor of Lennart Heimer (pp. 562–574). New York: New York Academy of Sciences.Google Scholar
Evans, G. W. (2003). A multimethodological analysis of cumulative risk and allostatic load among rural children. Developmental Psychology, 39, 924–933.CrossRefGoogle ScholarPubMed
Flaum, M., & Andreasen, N. C. (1995). Brain morphology in schizotypal personality as assessed by magnetic resonance imaging. In Raine, A., Lencz, T., & Mednick, S. A. (Eds.), Schizotypal personality disorder (pp. 385–405). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Gao, Y., Raine, A., Chan, F., Venables, P. H., & Mednick, S. A. (2010). Early maternal and paternal bonding, childhood physical abuse, and adult psychopathic personality. Psychological Medicine, 40, 1007–1016.CrossRefGoogle ScholarPubMed
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2010a). Association of poor childhood fear conditioning and adult crime. American Journal of Psychiatry, 167, 156–160.CrossRefGoogle ScholarPubMed
Gao, Y., Raine, A., Venables, P. H., Dawson, M. E., & Mednick, S. A. (2010b). Reduced electrodermal fear conditioning from ages 3 to 8 years is associated with aggressive behavior at age 8 years. Journal of Child Psychology and Psychiatry, 51, 550–558.CrossRefGoogle ScholarPubMed
Glenn, A. L., Raine, A., Venables, P. H., & Mednick, S. A. (2007). Early temperamental and psychophysiological precursors of adult psychopathic personality. Journal of Abnormal Psychology, 116, 508–518.CrossRefGoogle ScholarPubMed
Gould, E., & Tanapat, P. (1999). Stress and hippocampal neurogenesis. Biological Psychiatry, 46, 1472–1479.CrossRefGoogle ScholarPubMed
Gould, E., Tanapat, P., McEwen, B. S., Flugge, G., & Fuchs, E. (1998). Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proceedings of the National Academy of Sciences of the United States of America, 95, 3168–3171.CrossRefGoogle ScholarPubMed
Gruzelier, J., & Raine, A. (1994). Bilateral electrodermal activity and cerebral mechanisms in syndromes of schizophrenia and the schizotypal personality. International Journal of Psychophysiology, 16, 1–16.CrossRefGoogle ScholarPubMed
Gur, R., Turetsky, B., Cowell, P., Finkelman, C., Maany, V., Grossman, R., et al. (2000). Temporolimbic volume reductions in schizophrenia. Archives of General Psychiatry, 57, 769–775.CrossRefGoogle ScholarPubMed
Hazlett, E. A., Buchsbaum, M. S., Zhang, J., Newmark, R. E., Glanton, C. F., Zelmanova, Y., et al. (2008). Frontal–striatal–thalamic mediodorsal nucleus dysfunction in schizophrenia-spectrum patients during sensorimotor gating. NeuroImage, 42, 1164–1177.CrossRefGoogle ScholarPubMed
Hazlett, E. A., Levine, J., Buchsbaum, M. S., Silverman, J. M., New, A., et al. (2003). Deficient attentional modulation of the startle response in patients with schizotypal personality disorder. American Journal of Psychiatry, 160, 1621–1626.CrossRefGoogle ScholarPubMed
Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005). Limbic system mechanisms of stress regulation: Hypothalamo–pituitary–adrenocortical axis. Progress in Neuropsychopharmacology and Biological Psychiatry, 29, 1201–1213.CrossRefGoogle ScholarPubMed
Juster, R.-P., McEwen, B. S., & Lupien, S. J. (2010). Allostatic load biomarkers of chronic stress and impact on health and cognition. Neuroscience and Biobehavioral Reviews, 35, 2–16.CrossRefGoogle ScholarPubMed
Karlamangla, A. S., Singer, B. H., Greendale, G. A., & Seeman, T. E. (2005). Increase in epinephrine excretion is associated with cognitive decline in elderly men: MacArthur studies of successful aging. Psychoneuroendocrinology, 30, 453–460.CrossRefGoogle ScholarPubMed
Klosterkotter, J., Hellmich, M., Steinmeyer, E. M., & Schultze-Lutter, F. (2001). Diagnosing schizophrenia in the initial prodromal phase. Archives of General Psychiatry, 58, 158–164.CrossRefGoogle ScholarPubMed
Liddle, P. F., Friston, K. J., Frith, C. D., & Frackowiak, R. S. (1992). Cerebral blood flow and mental processes in schizophrenia. Journal of Research in Social Medicine, 85, 224–227.CrossRefGoogle ScholarPubMed
Liu, J., Raine, A., Venables, P. H., Dalais, C., & Mednick, S. A. (2003). Malnutrition at age 3 years and lower cognitive ability at age 11: Independence from social adversity. Archives of Pediatric and Adolescent Medicine, 157, 593–600.CrossRefGoogle Scholar
Liu, J. H., Raine, A., Venables, P. H., & Mednick, S. A. (2004). Malnutrition at age 3 years and externalizing behavior problems at ages 8, 11 and 17 years. American Journal of Psychiatry, 161, 2005–2013.CrossRefGoogle Scholar
Lupien, S. J., Ouellet-Morin, I., Hupbach, A., Tu, M. T., Buss, C., Walker, D., et al. (2006). Beyond the stress concept: Allostatic load—A developmental biological and cognitive perspective. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology (Vol. 2, 2nd ed., pp. 578–628). New York: Wiley.Google Scholar
Mason, O., Claridge, G., & Clark, K. (1997). Electrodermal relationships with personality measures of psychosis-proneness in psychotic and normal subjects. International Journal of Psychophysiology, 27, 137–146.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998a). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171–179.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1998b). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44.CrossRefGoogle ScholarPubMed
McEwen, B. S. (1999). Stress and hippocampal plasticity. Annual Review of Neuroscience, 22, 105–122.CrossRefGoogle ScholarPubMed
McEwen, B. S. (2000). Allostasis and allostatic load: Implications for neuropsychopharmacology. Neuropsychopharmacology, 22, 108–124.CrossRefGoogle ScholarPubMed
McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87, 873–904.CrossRefGoogle ScholarPubMed
McEwen, B. S. (2009). The brain is the central organ of stress and adaptation. NeuroImage, 47, 911–913.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Seeman, T. (1999). Protective and damaging effects of mediators of stress: Elaborating and testing the concepts of allostasis and allostatic load. Annals of the New York Academy Sciences, 896, 30–47.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Stellar, E. (1993). Stress and the individual: Mechanisms leading to disease. Archives of Internal Medicine, 153, 2093–2101.CrossRefGoogle ScholarPubMed
Mitchell, J. P., Banaji, M. R., & Macrae, C. N. (2005). The link between social cognition and self-referential thought in the medial prefrontal cortex. Journal of Cognitive Neuroscience, 17, 1306–1315.CrossRefGoogle ScholarPubMed
Modinos, G., Ormel, J., & Aleman, A. (2010). Altered activation and functional connectivity of neural systems supporting cognitive control of emotion in psychosis proneness. Schizophrenia Research, 118, 88–97.CrossRefGoogle ScholarPubMed
Mohanty, A., Herrington, J. D., Koven, N. S., Fisher, J. E., Wenzel, E. A., Webb, A. G., et al. 2005. Neural mechanisms of affective interference in schizotypy. Journal of Abnormal Psychology, 114, 16–27.CrossRefGoogle ScholarPubMed
Northoff, G., Heinzel, A., Greck, M., Bennpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain—A meta-analysis of imaging studies on the self. NeuroImage, 31, 440–457.CrossRefGoogle ScholarPubMed
Öhman, A., Hamm, A., & Hugdahl, K. (2000). Cognition and autonomic nervous system: Orienting, anticipation, and conditioning. In Cacioppo, J. T., Tassinary, L. G., & Berntson, G. (Eds.), Handbook of psychophysiology (2nd ed., pp. 533–575). New York: Cambridge University Press.Google Scholar
Raine, A. (1991). The SPQ-A scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin, 17, 555–564.CrossRefGoogle Scholar
Raine, A. (2006). Schizotypal personality: Neurodevelopmental and psychosocial trajectories. Annual Review of Clinical Psychology, 2, 291–326.CrossRefGoogle ScholarPubMed
Raine, A., Benishay, D., Lencz, T., & Scarpa, A. (1997). Abnormal orienting in schizotypal personality disorder. Schizophrenia Bulletin, 23, 75–82.CrossRefGoogle ScholarPubMed
Raine, A., Lencz, T., & Benishay, D. (1995). Schizotypal personality and skin conductance orienting. In Raine, A., Lencz, T., & Mednick, S. A. (Eds.), Schizotypal personality disorder (pp. 219–249). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Raine, A., Mellingen, K, Liu, J. H., Venables, P. H., & Mednick, S. A. (2003). Effects of environmental enrichment at 3–5 years on schizotypal personality and antisocial behavior at ages 17 and 23 years. American Journal of Psychiatry, 160, 1627–1635.CrossRefGoogle Scholar
Raine, A., Reynolds, C., Lencz, T., Scerbo, A., Triphon, N., & Kim, D. (1994). Cognitive–perceptual, interpersonal, and disorganized features of schizotypal personality. Schizophrenia ulletin, 20, 191–201.CrossRefGoogle ScholarPubMed
Raine, A., Reynolds, C., Venables, P. H., Mednick, S. A., & Farrington, D. P. (1998). Fearlessness, stimulation-seeking, and large body size at age 3 years as early predispositions to childhood aggression at age 11 years. Archives of General Psychiatry, 55, 745–751.CrossRefGoogle ScholarPubMed
Raine, A., Venables, P. H., Dalais, C., Mellingen, K., Reynolds, C., & Mednick, S. A. (2001). Early educational and health enrichment at age 3–5 years is associated with increased autonomic and central nervous system arousal and orienting at age 11 years: Evidence from the Mauritius Child Health Project. Psychophysiology, 38, 254–266.CrossRefGoogle ScholarPubMed
Raine, A., Venables, P. H., & Mednick, S. A. (1997). Low resting heart rate at age 3 years predisposes to aggression at age 11 years: Findings from the Mauritius Joint Child Health Project. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 1457–1464.CrossRefGoogle Scholar
Raine, A., Venables, P. H., Mednick, S. A., & Mellingen, K. (2002). Increased psychophysiological arousal and orienting at ages 3 and 11 years in persistently schizotypal adults. Schizophrenia Research, 54, 77–85.CrossRefGoogle ScholarPubMed
Reuben, D. B., Talvi, S. L. A., Rowe, J. W., & Seeman, T. E. (2000). High urinary catecholamine excretion predicts mortality and functional decline in high-functioning, community-dwelling older persons: MacArthur studies of successful aging. Journal of Gerontology, 55A, 618–624.Google Scholar
Reynolds, C. A., Raine, A., Mellingen, K., Venables, P. H., & Mednick, S. A. (2000). Three-factor model of schizotypal personality: Invariance across culture, gender, religious affiliation, family adversity, and psychopathology. Schizophrenia Bulletin, 26, 603–618.CrossRefGoogle ScholarPubMed
Salokangas, R. K. R., Heinimaa, M., Svirskis, T., Laine, T., Huttunen, J., Ristkari, T., et al. (2009). Perceived negative attitude of others as an early sign of psychosis. European Psychiatry, 24, 233–238CrossRefGoogle ScholarPubMed
Scarpa, A., Raine, A., Venables, P. H., & Mednick, S. A. (1997). Heart rate and skin conductance in behaviorally inhibited Mauritian children. Journal of Abnormal Psychology, 106, 182–190.CrossRefGoogle ScholarPubMed
Schulkin, J. (2003). Allostasis: A neural behavioral perspective. Hormones and Behavior, 43, 21–27.CrossRefGoogle ScholarPubMed
Seeman, T. E., & McEwen, B. S. (1996). Social environment characteristics and neuroendocrine function: The impact of social ties and support on neuroendocrine regulation. Psychosomatic Medicine, 58, 459–471.CrossRefGoogle ScholarPubMed
Sequeira, H., & Roy, J. C. (1993). Cortical and hypothalamo-limbic control of electrodermal responses. In Roy, J. C., Boucsein, W., Fowles, D. C., & Gruzelier, J. H. (Eds.), Progress in electrodermal research (pp. 93–114). New York: Plenum Press.CrossRefGoogle Scholar
Shonkoff, J. P., Boyce, W. T., & McEwen, B. S. (2009). Neuroscience, molecular biology, and the childhood roots of health disparities: Building a new framework for health promotion and disease prevention. Journal of the American Medical Association, 301, 2252–2259.CrossRefGoogle ScholarPubMed
Silbersweig, D. A., Stern, E., Frith, C. D., Cahill, C., Hommes, A., Grootoonk, S., et al. (1995). A functional neuroanatomy of hallucinations in schizophrenia. Nature, 378, 176–179.CrossRefGoogle ScholarPubMed
Singer, B., Ryff, C. D., & Seeman, T. (2004). Operationalizing allostatic load. In Schulkin, J. (Ed.), Allostasis, homeostasis, and the costs of physiological adaptation (pp. 113–149). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Sokolov, E. N. (1963). Perception and the conditioned reflex. Oxford: Pergamon Press.Google Scholar
Sterling, P., & Eyer, J. (1988). Allostasis: A new paradigm to explain arousal pathology. In: Fisher, S. & Reason, J. (Eds.), Handbook of life stress, cognition and health (pp. 629–649). New York: Wiley.Google Scholar
Suzuki, M., Zhou, S.-Y., Takahashi, T., Hagino, H., Kawasaki, Y., Niu, L., et al. (2005). Differential contributions of prefrontal and temporolimbic pathology to mechanisms of psychosis. Brain, 128, 2109–2122.CrossRefGoogle ScholarPubMed
Uno, H., Ross, T., Else, J., Suleman, M., & Sapolsky, R. (1989). Hippocampal damage associated with prolonged and fatal stress in primates. Journal of Neuroscience, 9, 1705–1711.CrossRefGoogle ScholarPubMed
Venables, P. H. (1978). Psychophysiology and psychometrics. Psychophysiology, 15, 302–315.CrossRefGoogle ScholarPubMed
Venables, P. H. (1993). Electrodermal indices as markers for the development of schizophrenia. In Roy, J. C., Boucsein, W., Fowles, D. C., & Gruzelier, J. H. (Eds.), Progress in electrodermal research (pp. 187–205). New York: Plenum Press.CrossRefGoogle Scholar
Vyas, A., Mitra, R., Rao, B. S. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience, 22, 6810–6818.CrossRefGoogle ScholarPubMed
Walker, E., Mittal, V., & Tessner, K. (2008). Stress and the hypothalamic pituitary adrenal axis in the developmental course of schizophrenia. Annual Review of Clinical Psychology, 4, 189–216.CrossRefGoogle ScholarPubMed
Wallin, B. G. (1981). Sympathetic nerve activity underlying electrodermal and cardiovascular reactions in man. Psychophysiology, 18, 470–476.CrossRefGoogle ScholarPubMed
Wang, J. J., Miyazato, H., Hokama, H., Hiramatsu, K., & Kondo, T. (2004). Correlation between P50 suppression and psychometric schizotypy among non-clinical Japanese subjects. International Journal of Psychophysiology, 52, 147–157.CrossRefGoogle ScholarPubMed
Weinberg, M. S., Johnson, D. C., Bhatt, A. P., & Spencer, R. L. (2010). Medial prefrontal cortex activity can disrupt the expression of stress response habituation. Neuroscience, 168, 744–756.CrossRefGoogle ScholarPubMed
Yung, A. R., & McGorry, P.D. (1996). The prodromal phase of first-episode psychosis: Past and current conceptualizations. Schizophrenia Bulletin, 22, 353–370.CrossRefGoogle ScholarPubMed