Hostname: page-component-5cf477f64f-qls9x Total loading time: 0 Render date: 2025-03-29T09:33:43.785Z Has data issue: false hasContentIssue false
  • English
  • Français

A multilevel prediction of physiological response to challenge: Interactions among child maltreatment, neighborhood crime, endothelial nitric oxide synthase gene (eNOS), and GABA(A) receptor subunit alpha-6 gene (GABRA6)

Published online by Cambridge University Press:  04 November 2015

Michael Lynch ,
Jody Todd Manly  and
Dante Cicchetti
Michael Lynch*
Affiliation:
State University of New York Geneseo
Jody Todd Manly
Affiliation:
University of Rochester Mt. Hope Family Center
Dante Cicchetti
Affiliation:
University of Minnesota Institute of Child Development
*
Address correspondence and reprint requests to: Michael Lynch, Department of Psychology, State University of New York Geneseo, 1 College Circle, Geneseo, NY 14454. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Physiological response to stress has been linked to a variety of healthy and pathological conditions. The current study conducted a multilevel examination of interactions among environmental toxins (i.e., neighborhood crime and child maltreatment) and specific genetic polymorphisms of the endothelial nitric oxide synthase gene (eNOS) and GABA(A) receptor subunit alpha-6 gene (GABRA6). One hundred eighty-six children were recruited at age 4. The presence or absence of child maltreatment as well as the amount of crime that occurred in their neighborhood during the previous year were determined at that time. At age 9, the children were brought to the lab, where their physiological response to a cognitive challenge (i.e., change in the amplitude of the respiratory sinus arrhythmia) was assessed and DNA samples were collected for subsequent genotyping. The results confirmed that complex Gene × Gene, Environment × Environment, and Gene × Environment interactions were associated with different patterns of respiratory sinus arrhythmia reactivity. The implications for future research and evidence-based intervention are discussed.

Type
Regular Articles
Information
Development and Psychopathology , Volume 27 , Special Issue 4pt2: Multilevel Developmental Perspectives on Child Maltreatment , November 2015 , pp. 1471 - 1487
Copyright
Copyright © Cambridge University Press 2015 

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

Aber, J. L., Jones, S. M., Brown, J. A., Chaudry, N., & Samples, F. (1998). Resolving conflict creatively: Evaluating the developmental effects of a school-based violence prevention program in neighborhood and classroom context. Development and Psychopathology, 10, 187–213.Google Scholar
Arias, B., Aguilera, M., Moya, J., Sáiz, P. A., Villa, H., Ibáñez, M. I., et al. (2012). The role of genetic variability in the SLC6A4, BDNF and GABRA6 genes in anxiety-related traits. Acta Psychiatrica Scandinavica, 125, 194–202.Google Scholar
Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. In Cicchetti, D. & Toth, S. L. (Eds.), Child abuse, child development, and social policy (pp. 7–73). Norwood, NJ: Ablex.Google Scholar
Beauchaine, T. (2001). Vagal tone, development, and Gray's motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183–214.Google Scholar
Beauchaine, T., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74, 174–184.Google Scholar
Belsky, J. (1980). Child maltreatment: An ecological integration. American Psychologist, 35, 320–335.Google Scholar
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908.CrossRefGoogle ScholarPubMed
Binkley, P. F., Nuziatta, E., Liu-Stratton, Y., & Cooke, G. (2005). A polymorphism of the endothelial nitric oxide synthase promoter is associated with an increase in autonomic imbalance in patients with congestive heart failure. American Heart Journal, 149, 342–348.CrossRefGoogle ScholarPubMed
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., & Kuppfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144–150.Google Scholar
Bronfenbrenner, U. (1977). Toward an experimental ecology of human development. American Psychologist, 32, 513–531.Google Scholar
Butler, E. A., Wilhelm, F. H., & Gross, J. J. (2006). Respiratory sinus arrhythmia, emotion, and emotion regulation during social interaction. Psychophysiology, 43, 612–622.Google Scholar
Calkins, S. D., Graziano, P., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144–153.CrossRefGoogle ScholarPubMed
Calkins, S. D., Smith, C. L., Gill, K., & Johnson, M. C. (1998). Maternal interactive style across contexts: Relations to emotional, behavioral and physiological regulation during toddlerhood. Social Development, 7, 350–369.CrossRefGoogle Scholar
Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry, 167, 509–527.Google Scholar
Chaffin, M., Funderburk, B., Bard, D., Valle, L. A., & Gurwitch, R. (2011). A combined motivation and parent-child interaction therapy package reduces child welfare recidivism in a randomized dismantling field trial. Journal of Consulting and Clinical Psychology, 79, 84–95.Google Scholar
Chida, Y., & Hamer, M. (2008). Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: A quantitative review of 30 years of investigations. Psychological Bulletin, 134, 829–885.Google Scholar
Cicchetti, D., & Lynch, M. (1995). Failures in the expectable environment and their impact on individual development: The case of child maltreatment. In Cicchetti, D. & Cohen, D. J. (Eds.), Developmental psychopathology: Vol. 2. Risk, disorder, and adaptation (pp. 32–71). New York: Wiley.Google Scholar
Cicchetti, D., & Valentino, K. (2006). An ecological-transactional perspective on child maltreatment: Failure of the average expectable environment and its influence on child development. In Cicchetti, D. & Cohen, D. (Eds.), Development and psychopathology: Risk, disorder, and adaptation (2nd ed., Vol. 3, pp. 129–201). New York: Wiley.Google Scholar
Conradt, E., Degarmo, D., Fisher, P., Abar, B., Lester, B. M., Lagasse, L. L., et al. (2014). The contributions of early adverse experiences and trajectories of respiratory sinus arrhythmia on the development of neurobehavioral disinhibition among children with prenatal substance exposure. Development and Psychopathology, 26, 901–916.CrossRefGoogle ScholarPubMed
Cooley-Quille, M., Boyd, R. C., Frantz, F., & Walsh, J. (2001). Emotional and behavioral impact of exposure to community violence in inner-city adolescents. Journal of Community Psychology, 30, 199–206.Google Scholar
Coulton, C., Korbin, J., Su, M., & Chow, J. (1995). Community level factors and child maltreatment rates. Child Development, 66, 1262–1276.Google Scholar
Culotta, E., & Koshland, D. E. (1992). NO news is good news. Science, 258, 1862–1864.Google Scholar
Dale, L. P., Carroll, L. E., Galen, G., Hayes, J. A., Webb, K.W., & Porges, S. W. (2009). Abuse history is related to autonomic regulation to mild exercise and psychological wellbeing. Applied Psychophysiology Biofeedback, 34, 299–308.CrossRefGoogle ScholarPubMed
De Geus, E. J. C., & Van Doornen, L. J. P. (1996). Ambulatory assessment of parasympathetic/sympathetic balance by impedance cardiography. In Fahrenberg, J. & Myrtek, M. (Eds.), Ambulatory assessment: Computer assisted psychological and psychophysiological methods in monitoring and field studies (pp. 141–164). Berlin: Hogrefe & Huber.Google Scholar
Demas, G. E., Kriegsfeld, L. J., Blackshaw, S., Huang, P. L., Gammie, S. C., Nelson, R. J., et al. (1999). Elimination of aggressive behavior in male mice lacking endothelial nitric oxide synthase. Journal of Neuroscience, 19, 1–5.CrossRefGoogle ScholarPubMed
Denver, J. W., Reed, S. F., & Porges, S. W. (2007). Methodological issues in the quantification of respiratory sinus arrhythmia. Biological Psychology, 74, 286–294.Google Scholar
Duncan, C. E., Webster, M. J., Rothmond, D. A., Bahn, S., Elashoff, M., & Shannon Weickert, C. (2010). Prefrontal GABA(A) receptor alpha-subunit expression in normal postnatal human development and schizophrenia. Journal of Psychiatric Research, 44, 673–681.CrossRefGoogle ScholarPubMed
Eaves, L., Foley, D., & Silberg, J. (2003). Has the “equal environments” assumption been tested in twin studies? Twin Research, 6, 486–489.Google Scholar
Eisenberg, N., Fabes, R. A., Karbon, M., Murphy, B. C., Wosinski, M., Polazzi, L., et al. (1996). The relations of children's dispositional prosocial behavior to emotionality, regulation, and social functioning. Child Development, 67, 974–992.CrossRefGoogle ScholarPubMed
Ellis, B. J., Essex, M. J., & Boyce, W. T. (2005). Biological sensitivity to context: II. Empirical explorations of an evolutionary–developmental theory. Development and Psychopathology, 17, 303–328.Google ScholarPubMed
El-Sheikh, M., Hinnant, J. B., & Erath, S. (2011). Developmental trajectories of delinquency symptoms in childhood: The role of marital conflict and autonomic nervous system activity. Journal of Abnormal Psychology, 120, 16–32.Google Scholar
El-Sheikh, M., Kouros, C. D., Erath, S., Cummings, E. M., Keller, P., Staton, L., et al. (2009). Marital conflict and children's externalizing behavior: Interactions between parasympathetic and sympathetic nervous system activity. Monographs of the Society for Research in Child Development, 74, 1–69.Google ScholarPubMed
Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.Google Scholar
Falush, D., Stephens, M., & Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: Dominant and null alleles. Molecular Ecology Notes, 7, 574–578.Google Scholar
Frost, R., & Stauffer, J. (1987). The effects of social class, gender, and personality on physiological responses to filmed violence. Journal of Communication, 37, 29–45.CrossRefGoogle Scholar
Gaudin, J. M. (1999). Child neglect: Short-term and long-term consequences. In Dubowitz, H. (Ed.), Neglected children: Research, practice, and policy (pp. 89–108). Thousand Oaks, CA: Sage.Google Scholar
Gordis, E. B., Feres, N., Olezeski, C. L., Rabkin, A. N., & Trickett, P. K. (2010). Skin conductance reactivity and respiratory sinus arrhythmia among maltreated and comparison youth: Relations with aggressive behavior. Journal of Pediatric Psychology, 35, 547–558.Google Scholar
Greaves-Lord, K., Tulen, J., Dietrich, A., Sondeijker, F., van Roon, A., Oldehinkel, A., et al. (2010). Reduced autonomic flexibility as a predictor for future anxiety in girls from the general population: The TRAILS study. Psychiatry Research, 179, 187–193.Google Scholar
Hakman, M., Chaffin, M., Funderburk, B., & Silovsky, J. F. (2009). Change trajectories for parent-child interaction sequences during parent-child interaction therapy for child physical abuse. Child Abuse & Neglect, 33, 461–470.Google Scholar
Han, D. H., Bolo, N., Daniels, M. A., Lyoo, I. K., Min, K. J., Kim, C. H., et al. (2008). Craving for alcohol and food during treatment for alcohol dependence: Modulation by T allele of 1519T > C GABAAalpha6. Alcoholism, Clinical and Experimental Research, 32, 1593–1599.Google Scholar
Haul, S., Godecke, A., Schrader, J., Haas, H. L., & Luhmann, H. J. (1999). Impairment of neocortical long-term potentiation in mice deficient of endothelial nitric oxide synthase. Journal of Neurophysiology, 81, 494–497.CrossRefGoogle ScholarPubMed
Heim, C., Newport, D. J., Heit, S., Graham, Y. P., Wilcox, M., Bonsall, R., et al. (2000). Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. Journal of the American Medical Association, 284, 592–597.Google Scholar
Hill-Soderlund, A. L., Mills-Koonce, W. R., Propper, C., Calkins, S. D., Granger, D. A., Moore, G. A., et al. (2008). Parasympathetic and sympathetic responses to the strange situation in infants and mothers from avoidant and securely attached dyads. Developmental Psychobiology, 50, 361–376.Google Scholar
Huang, P. L., Huang, Z., Mashimo, H., Bloch, K. D., Moskowitz, M. A., Bevan, J. A., et al. (1995). Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature, 377, 239–242.Google Scholar
Hubisz, M. J., Falush, D., Stephens, M., & Pritchard, J. K. (2009). Inferring weak population structure with assistance of sample group information. Molecular Ecology Resources, 5, 1322–1332.Google Scholar
Huffman, L. C., Bryan, Y., Del Carmen, R., Pederson, F., Doussard-Roosevelt, J., & Porges, S. W. (1998). Infant temperament and cardiac vagal tone: Assessments at twelve weeks of age. Child Development, 69, 624–635.Google Scholar
Jacobson, N. S., Gottman, J. M., Shortt, J. W., & Wu, J. (1995). The distinction between Type 1 and Type 2 batterers—Further considerations: Reply to Ornduff et al. (1995), Margolin et al. (1995), and Walker (1995). Journal of Family Psychology, 9, 272–279.Google Scholar
Kano, T., Shimizu-Sasamata, M., Huang, P. L., Moskowitz, M. A., & Lo, E. H. (1998). Effects of nitric oxide synthase gene knockout on neurotransmitter release in vivo. Neuroscience, 86, 695–699.Google Scholar
Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011). The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: Evidence of genetic moderation. Archives of General Psychiatry, 68, 444–454.Google Scholar
Katz, L. F. (2007). Domestic violence and vagal reactivity to peer provocation. Biological Psychology, 74, 154–164.Google Scholar
Keller, M. C. (2014). Gene x environment interaction studies have not properly controlled for potential confounders: The problem and the (simple) solution. Biological Psychiatry, 75, 18–24.Google Scholar
Kemp, A. H., Quintana, D. S., Gray, M. A., Felmingham, K. L., Brown, K., & Gatt, J. M. (2010). Impact of depression and antidepressant treatment on heart rate variability: A review and meta-analysis. Biological Psychiatry, 67, 1067–1074.Google Scholar
Key, B. L., Campbell, T. S., Bacon, S. L., & Gerin, W. (2008). The influence of trait and state rumination on cardiovascular recovery from a negative emotional stressor. Journal of Behavioral Medicine, 31, 237–248.Google Scholar
Korbin, J. E., Coulton, C. J., Chard, S., Platt-Houston, C., & Su, M., (1998). Impoverishment and child maltreatment in African American and European American neighborhoods. Development and Psychopathology, 10, 215–233.Google Scholar
Krenichyn, K., Saegert, S., & Evans, G. W. (2001). Parents as moderators of psychological and physiological correlates of inner-city children's exposure to violence. Applied Developmental Psychology, 22, 581–602.Google Scholar
Kwong, M., Bartholomew, K., Henderson, A., & Trinke, S. (2003). The intergenerational transmission of relationship violence. Journal of Family Psychology, 17, 288–301.Google Scholar
Lai, C. Q., Tucker, K. L., Choudhry, S., Parnell, L. D., Mattei, J., Garcia-Bailo, B., et al. (2009). Population admixture associated with disease prevalence in the Boston Puerto Rican health study. Human Genetics, 125, 199–205.Google Scholar
Lehrer, P., Smetankin, A., & Potapova, T. (2000). Respiratory sinus arrhythmia biofeedback therapy for asthma: A report of 20 unmedicated pediatric cases using the Smetankin Method. Applied Psychophysiology and Biofeedback, 24, 193–200.Google Scholar
Lewis, G. F., Furman, S. A., McCool, M. F., & Porges, S. W. (2012). Statistical strategies to quantify respiratory sinus arrhythmia: Are commonly used metrics equivalent? Biological Psychology, 89, 349–364.CrossRefGoogle ScholarPubMed
Manly, J. T. (2005). Invited commentary: Advances in research definitions of child maltreatment. Child Abuse and Neglect, 29, 413–619.Google Scholar
McEwen, B. S. (2003). Mood disorders and allostatic load. Biological Psychiatry, 54, 200–207.CrossRefGoogle ScholarPubMed
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15.CrossRefGoogle ScholarPubMed
Mehta, D., & Binder, E. B. (2012). Gene x environment vulnerability factors for PTSD: The HPA-axis. Neuropharmacology, 62, 654–662.Google Scholar
Miskovic, V., Schmidt, L. A., Georgiades, K., Boyle, M., & MacMillan, H. L. (2009). Stability of resting frontal electroencephalogram (EEG) asymmetry and cardiac vagal tone in adolescent females exposed to child maltreatment. Developmental Psychobiology, 51, 474–487.Google Scholar
Movius, H. L., & Allen, J. J. B. (2005). Cardiac vagal tone, defensiveness, and motivational style. Biological Psychology, 68, 147–162.Google Scholar
Nunes, R. A. B., Barroso, L. P., Pereira, A. da C., Krieger, J. E., & Mansur, A. J. (2014). Gender-related associations of genetic polymorphisms of α-adrenergic receptors, endothelial nitric oxide synthase and bradykinin B2 receptor with treadmill exercise test responses. Open Heart, 1, e000132.Google Scholar
Obradović, J., Bush, N. R., Stamperdahl, J., Adler, N. E., & Boyce, W. T. (2010). Biological sensitivity to context: The interactive effects of stress reactivity and family adversity on socioemotional behavior and school readiness. Child Development, 81, 270–289.Google Scholar
Oosterman, M., de Schipper, J. C., Fisher, P., Dozier, M., & Schuengel, C. (2010). Autonomic reactivity in relation to attachment and early adversity among foster children. Development and Psychopathology, 22, 109–118.Google Scholar
Ottaviani, C., Shapiro, D., Davydov, D. M., & Goldstein, I. B. (2008). Autonomic stress response modes and ambulatory heart rate level and variability. Journal of Psychophysiology, 22, 28–40.Google Scholar
Porges, S. W. (1985). Method and apparatus for evaluating rhythmic oscillations in aperiodic physiological response systems. Patent No. 4,510,944. Washington DC: US Patent Office.Google Scholar
Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage: A polyvagal theory. Psychophysiology, 32, 301–318.Google Scholar
Porges, S. W. (1998). Love: An emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology, 23, 837–861.Google Scholar
Porges, S. W. (2001). The polyvagal theory: Phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146.Google Scholar
Porges, S. W. (2004). Neuroception: A subconscious system for detecting threat and safety. Zero to Three: Bulletin of the National Center for Clinical Infant Programs, 24, 19–24.Google Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143.Google Scholar
Porges, S. W., & Bohrer, R. E. (1990). Analyses of periodic processes in psychophysiological research. In Cacioppo, J. T. & Tassinary, L. G. (Eds.), Principles of psychophysiology: physical, social, and inferential elements (pp. 708–753). New York: Cambridge University Press.Google Scholar
Porges, S. W., & Byrne, E. A. (1992). Research methods for measurement of heart rate and respiration. Biological Psychology, 34, 93–130.Google Scholar
Porges, S. W., Doussard-Roosevelt, J. A., Portales, A. L., & Greenspan, S. I. (1996). Infant regulation of the vagal “brake” predicts child behavior problems: A psychobiological model of social behavior. Developmental Psychobiology, 29, 697–712.Google Scholar
Posner, M. I., & Rothbart, M. K. (2000). Developing mechanisms of self-regulation. Development and Psychopathology, 12, 427–441.Google Scholar
Propper, C., & Moore, G. A. (2006). The influence of parenting on infant emotionality: A multi-level psychobiological perspective. Developmental Review, 26, 427–460.Google Scholar
Randin, D., Vollenweider, P., Tappy, L., Jéquier, E., Nicod, P., & Scherrer, U. (1995). Suppression of alcohol-induced hypertension by dexamethasone. New England Journal of Medicine, 332, 1733–1737.CrossRefGoogle ScholarPubMed
Rigterink, T., Katz, L. F., & Hessler, D. M. (2010). Domestic violence and longitudinal associations with children's physiological regulation abilities. Journal of Interpersonal Violence, 25, 1669–1683.Google Scholar
Riniolo, T. C., & Porges, S. W. (1997). Inferential and descriptive influences on measures of respiratory sinus arrhythmia: Sampling rate, r-wave trigger accuracy, and variance estimates. Psychophysiology, 34, 613–621.CrossRefGoogle ScholarPubMed
Samerfoff, A., & Chandler, M. (1975). Reproductive risk and the continuum of caretaking casualty. In Horowitz, F. (Ed.), Review of child development research (Vol. 4, pp. 187–244). Chicago: University of Chicago Press.Google Scholar
Sedlak, A. J., Mettenburg, J., Basena, M., Petta, I., McPherson, K., Greene, A., et al. (2010). Fourth National Incidence Study of Child Abuse and Neglect (NIS–4): Report to Congress. Washington, DC: US Department of Health and Human Services, Administration for Children and Families.Google Scholar
Shankarishan, P., Borah, P. K., Ahmed, G., & Mahanta, J. (2014). Endothelial nitric oxide synthase gene polymorphisms and the risk of hypertension in an Indian population. BioMed Research International, Article 793040.Google Scholar
Shenk, C. E., Noll, J. G., Putnam, F. W., & Trickett, P. K. (2010). A prospective examination of the role of childhood sexual abuse and physiological asymmetry in the development of psychopathology. Child Abuse and Neglect, 34, 752–761.Google Scholar
Skowron, E. A., Loken, E., Gatzke-Kopp, L. M., Cipriano-Essel, E. A., Woehrle, P. L., Van Epps, J. J., et al. (2011). Mapping cardiac physiology and parenting processes in maltreating mother-child dyads. Journal of Family Psychology, 25, 663–674.Google Scholar
Skowron, E. A., & Reinneman, D. H. S. (2005). Psychological interventions for child maltreatment: A meta-analysis. Psychotherapy: Theory, Research, Practice, and Training, 42, 52–71.Google Scholar
Thayer, J. F., Friedman, B. H., & Borkovec, T. D. (1996). Autonomic characteristics of generalized anxiety disorder and worry. Biological Psychiatry, 39, 255–266.Google Scholar
Uhart, M., McCaul, M. E., Oswald, L. M., Choi, L., & Wand, G. S. (2004). GABRA6 gene polymorphism and an attenuated stress response. Molecular Psychiatry, 9, 998–1006.CrossRefGoogle Scholar
Watanabe, M., Maemura, K., Kanbara, K., Tamayama, T., & Hayasaki, H. (2002). GABA and GABA receptors in the central nervous system and other organs. International Review of Cytology, 213, 1–47.Google Scholar
Waugh, C. E., Panage, S., Mendes, W. B., & Gotlib, I. H. (2010). Cardiovascular and affective recovery from anticipatory threat. Biological Psychology, 84, 169–175.Google Scholar
Wilson, D., Kliewer, W., Teasley, N., Plybon, L., & Sica, D. (2002). Violence exposure, catecholamine excretion, and blood pressure non-dipping status in African-American male versus female adolescents. Psychosomatic Medicine, 64, 906–915.Google Scholar
Wilson, R. I., Godecke, A., Brown, R. E., Schrader, J., & Haas, H. L. (1999). Mice deficient in endothelial nitric oxide synthase exhibit a selective deficit in hippocampal long-term potentiation. Neuroscience, 90, 1157–1165.Google Scholar
Yaeger, R., Alvial-Bront, A., Abdul, K., Nolan, P. C., Grann, V. R., Birchette, M. G., et al. (2008). Comparing genetic ancestry and self-described race in African Americans born in the United States and in Africa. Cancer Epidemiology, Biomarkers & Prevention, 17, 1329–1338.Google Scholar
Yamada, Y., Noborisaka, Y., Ishizaki, M., Tsuritani, I., Honda, R., & Yamada, S. (2004). Alcohol consumption, homeostasis model assessment indices and blood pressure in middle-aged healthy men. Journal of Human Hypertension, 18, 343–350.Google Scholar
Yasuma, F., & Hayano, J.-I. (2004). Respiratory sinus arrhythmia: Why does the heartbeat synchronize with respiratory rhythm? Chest, 125, 683–690.Google Scholar
Zucker, T. L., Samuelson, K. W., Muench, F., Greenberg, M. A., & Gevirtz, R. N. (2009). The effects of respiratory sinus arrhythmia biofeedback on heart rate variability and posttraumatic stress disorder symptoms: A pilot study. Applied Psychophysiology and Biofeedback, 34, 135–143.Google Scholar