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Gepubliceerd in: Research on Child and Adolescent Psychopathology 8/2015

29-07-2015

Variation in Parasympathetic Dysregulation Moderates Short-term Memory Problems in Childhood Attention-Deficit/Hyperactivity Disorder

Auteurs: Anthony R. Ward, Gabriela Alarcón, Joel T. Nigg, Erica D. Musser

Gepubliceerd in: Research on Child and Adolescent Psychopathology | Uitgave 8/2015

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Abstract

Although attention deficit/hyperactivity disorder (ADHD) is associated with impairment in working memory and short-term memory, up to half of individual children with ADHD perform within a normative range. Heterogeneity in other ADHD-related mechanisms, which may compensate for or combine with cognitive weaknesses, is a likely explanation. One candidate is the robustness of parasympathetic regulation (as indexed by respiratory sinus arrhythmia; RSA). Theory and data suggest that a common neural network is likely tied to both heart-rate regulation and certain cognitive functions (including aspects of working and short-term memory). Cardiac-derived indices of parasympathetic reactivity were collected during short-term memory (STM) storage and rehearsal tasks from 243 children (116 ADHD, 127 controls). ADHD was associated with lower STM performance, replicating previous work. In addition, RSA reactivity moderated the association between STM and ADHD – both as a category and a dimension – independent of comorbidity. Specifically, conditional effects revealed that high levels of withdrawal interacted with weakened STM but high levels of augmentation moderated a positive association predicting ADHD. Thus, variations in parasympathetic reactivity may help explain neuropsychological heterogeneity in ADHD.
Voetnoten
1
Extant work has suggested that many commonly used simple span tasks such as those used here consistently load on a factor typically referred to as short-term memory (i.e., storage or rehearsal abilities) while more complex tasks better index working memory (see Engle 2002). However, as evidenced in meta-analytic literature (Martinussen et al. 2005; Willcutt et al. 2005), these simple span tasks are often employed as measures of working memory. Thus, to increase the generalizability of findings to previous studies, we utilize simple span tasks but have chosen to use the terms short-term memory storage and rehearsal to reflect this advancement.
 
2
Moderation analyses were also conducted using ADHD Inattentive and Combined presentations as categorical outcomes. Findings largely mirrored those presented here and below. Specific findings are available upon request.
 
Literatuur
go back to reference American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington: American Psychiatric Publishing.CrossRef American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington: American Psychiatric Publishing.CrossRef
go back to reference American Psychological Association. (2002). Ethical principles of psychologists and code of conduct. American Psychologist, 57, 1060–1073.CrossRef American Psychological Association. (2002). Ethical principles of psychologists and code of conduct. American Psychologist, 57, 1060–1073.CrossRef
go back to reference Arnsten, A. F., & Li, B. M. (2005). Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biological Psychiatry, 57, 1377–1384.CrossRefPubMed Arnsten, A. F., & Li, B. M. (2005). Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biological Psychiatry, 57, 1377–1384.CrossRefPubMed
go back to reference Baddeley, A. D. (2007). Working memory, thought and action. Oxford: Oxford Univ. Press.CrossRef Baddeley, A. D. (2007). Working memory, thought and action. Oxford: Oxford Univ. Press.CrossRef
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
go back to reference Beauchaine, T. P., Katkin, E. S., Strassberg, Z., & Snarr, J. (2001). Disinhibitory psychopathology in male adolescents: discriminating conduct disorder from attention-deficit/hyperactivity disorder through concurrent assessment of multiple autonomic states. Journal of Abnormal Psychology, 110, 610–624.CrossRefPubMed Beauchaine, T. P., Katkin, E. S., Strassberg, Z., & Snarr, J. (2001). Disinhibitory psychopathology in male adolescents: discriminating conduct disorder from attention-deficit/hyperactivity disorder through concurrent assessment of multiple autonomic states. Journal of Abnormal Psychology, 110, 610–624.CrossRefPubMed
go back to reference Biederman, J., Monuteaux, M. C., Doyle, A. E., Seidman, L. J., Wilens, T. E., Ferrero, F., … & Faraone, S. V. (2004). Impact of executive function deficits and attention-deficit/hyperactivity disorder (ADHD) on academic outcomes in children. Journal of Consulting and Clinical Psychology, 72, 757. Biederman, J., Monuteaux, M. C., Doyle, A. E., Seidman, L. J., Wilens, T. E., Ferrero, F., … & Faraone, S. V. (2004). Impact of executive function deficits and attention-deficit/hyperactivity disorder (ADHD) on academic outcomes in children. Journal of Consulting and Clinical Psychology, 72, 757.
go back to reference Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144–153.CrossRefPubMed Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74, 144–153.CrossRefPubMed
go back to reference Cantor, J., Engle, R. W., & Hamilton, G. (1991). Short-term memory, working memory, and verbal abilities: how do they relate? Intelligence, 15, 229–246.CrossRef Cantor, J., Engle, R. W., & Hamilton, G. (1991). Short-term memory, working memory, and verbal abilities: how do they relate? Intelligence, 15, 229–246.CrossRef
go back to reference Cohen, J., Cohen, P., West, S. G., & Aiken, L. S. (2003). Applied multiple regression/correlation analysis for the behavioral sciences. Mahwah: Lawrence Erlbaum Associates. Cohen, J., Cohen, P., West, S. G., & Aiken, L. S. (2003). Applied multiple regression/correlation analysis for the behavioral sciences. Mahwah: Lawrence Erlbaum Associates.
go back to reference Conradt, E., Degarmo, D., Fisher, P., Abar, B., Lester, B. M., Lagasse, L. L., … & Hammond, J. A. (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. Conradt, E., Degarmo, D., Fisher, P., Abar, B., Lester, B. M., Lagasse, L. L., … & Hammond, J. A. (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.
go back to reference Conway, A. R., Kane, M. J., Bunting, M. F., Hambrick, D. Z., Wilhelm, O., & Engle, R. W. (2005). Working memory span tasks: a methodological review and user’s guide. Psychonomic Bulletin & Review, 12, 769–786.CrossRef Conway, A. R., Kane, M. J., Bunting, M. F., Hambrick, D. Z., Wilhelm, O., & Engle, R. W. (2005). Working memory span tasks: a methodological review and user’s guide. Psychonomic Bulletin & Review, 12, 769–786.CrossRef
go back to reference Crowell, S. E., Beauchaine, T. P., Gatzke-Kopp, L., Sylvers, P., Mead, H., & Chipman-Chacon, J. (2006). Autonomic correlates of attention-deficit/hyperactivity disorder and oppositional defiant disorder in preschool children. Journal of Abnormal Psychology, 115, 174.CrossRefPubMed Crowell, S. E., Beauchaine, T. P., Gatzke-Kopp, L., Sylvers, P., Mead, H., & Chipman-Chacon, J. (2006). Autonomic correlates of attention-deficit/hyperactivity disorder and oppositional defiant disorder in preschool children. Journal of Abnormal Psychology, 115, 174.CrossRefPubMed
go back to reference DuPaul, G. J., Power, T. J., Anastopoulos, A. D., & Reid, R. (1998). ADHD rating scale—IV: Checklists, norms, and clinical interpretation. New York: Guilford Press. DuPaul, G. J., Power, T. J., Anastopoulos, A. D., & Reid, R. (1998). ADHD rating scale—IV: Checklists, norms, and clinical interpretation. New York: Guilford Press.
go back to reference Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11, 19–23.CrossRef Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11, 19–23.CrossRef
go back to reference Engle, R. W., Tuholski, S. W., Laughlin, J. E., & Conway, A. R. (1999). Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. Journal of Experimental Psychology: General, 128, 309.CrossRef Engle, R. W., Tuholski, S. W., Laughlin, J. E., & Conway, A. R. (1999). Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. Journal of Experimental Psychology: General, 128, 309.CrossRef
go back to reference Fray, P. J., Robbins, T. W., & Sahakian, B. J. (1996). Neuropsychiatric applications of CANTAB. International Journal of Geriatric Psychiatry, 11, 329–336.CrossRef Fray, P. J., Robbins, T. W., & Sahakian, B. J. (1996). Neuropsychiatric applications of CANTAB. International Journal of Geriatric Psychiatry, 11, 329–336.CrossRef
go back to reference Froehlich, T. E., Lanphear, B. P., Epstein, J. N., Barbaresi, W. J., Katusic, S. K., & Kahn, R. S. (2007). Prevalence, recognition, and treatment of attention-deficit/hyperactivity disorder in a national sample of U.S. children. Archives of Pediatrics & Adolescent Medicine, 161, 857–864.CrossRef Froehlich, T. E., Lanphear, B. P., Epstein, J. N., Barbaresi, W. J., Katusic, S. K., & Kahn, R. S. (2007). Prevalence, recognition, and treatment of attention-deficit/hyperactivity disorder in a national sample of U.S. children. Archives of Pediatrics & Adolescent Medicine, 161, 857–864.CrossRef
go back to reference Gianaros, P. J., Van der Veen, F. M., & Jennings, J. R. (2004). Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology, 41, 521–530. doi:10.1111/1469-8986.2004.00179.x.CrossRefPubMedPubMedCentral Gianaros, P. J., Van der Veen, F. M., & Jennings, J. R. (2004). Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology, 41, 521–530. doi:10.​1111/​1469-8986.​2004.​00179.​x.CrossRefPubMedPubMedCentral
go back to reference Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children’s adaptive functioning: a meta-analysis. Biological Psychology, 94, 22–37.CrossRefPubMedPubMedCentral Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children’s adaptive functioning: a meta-analysis. Biological Psychology, 94, 22–37.CrossRefPubMedPubMedCentral
go back to reference Gropper, R. J., & Tannock, R. (2009). A pilot study of working memory and academic achievement in college students with ADHD. Journal of Attention Disorders, 12, 574–581.CrossRefPubMed Gropper, R. J., & Tannock, R. (2009). A pilot study of working memory and academic achievement in college students with ADHD. Journal of Attention Disorders, 12, 574–581.CrossRefPubMed
go back to reference Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press. Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.
go back to reference Hsieh, F. Y. (1989). Sample size tables for logistic regression. Statistics in Medicine, 8, 795–802.CrossRefPubMed Hsieh, F. Y. (1989). Sample size tables for logistic regression. Statistics in Medicine, 8, 795–802.CrossRefPubMed
go back to reference Jensen, A. R., & Figueroa, R. A. (1975). Forward and backward digit span interaction with race and IQ: predictions from Jensen’s theory. Journal of Educational Psychology, 67, 882.CrossRefPubMed Jensen, A. R., & Figueroa, R. A. (1975). Forward and backward digit span interaction with race and IQ: predictions from Jensen’s theory. Journal of Educational Psychology, 67, 882.CrossRefPubMed
go back to reference Loeber, R., Green, S., Lahey, B., Frick, P., & McBurnett, K. (2000). Findings on disruptive behavior disorders from the first decade of the developmental trends study. Clinical Child and Family Psychology Review, 3, 37–60. doi:10.1023/A:1009567419190.CrossRefPubMed Loeber, R., Green, S., Lahey, B., Frick, P., & McBurnett, K. (2000). Findings on disruptive behavior disorders from the first decade of the developmental trends study. Clinical Child and Family Psychology Review, 3, 37–60. doi:10.​1023/​A:​1009567419190.CrossRefPubMed
go back to reference Marcovitch, S., Leigh, J., Calkins, S. D., Leerks, E. M., O’Brien, M., & Blankson, A. N. (2010). Moderate vagal withdrawal in 3.5‐year‐old children is associated with optimal performance on executive function tasks. Developmental Psychobiology, 52, 603–608. doi:10.1002/dev.20462.CrossRefPubMedPubMedCentral Marcovitch, S., Leigh, J., Calkins, S. D., Leerks, E. M., O’Brien, M., & Blankson, A. N. (2010). Moderate vagal withdrawal in 3.5‐year‐old children is associated with optimal performance on executive function tasks. Developmental Psychobiology, 52, 603–608. doi:10.​1002/​dev.​20462.CrossRefPubMedPubMedCentral
go back to reference Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 377.CrossRefPubMed Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 377.CrossRefPubMed
go back to reference MindWare. (2008). MindWare heart rate variability V. 2.6 system. Gahanna: MindWare Technologies. MindWare. (2008). MindWare heart rate variability V. 2.6 system. Gahanna: MindWare Technologies.
go back to reference Musser, E. D., Backs, R. W., Schmitt, C. F., Ablow, J. C., Measelle, J. R., & Nigg, J. T. (2011). Emotion regulation via the autonomic nervous system in children with attention-deficit/hyperactivity disorder (ADHD). Journal of Abnormal Child Psychology, 39, 841–852. Musser, E. D., Backs, R. W., Schmitt, C. F., Ablow, J. C., Measelle, J. R., & Nigg, J. T. (2011). Emotion regulation via the autonomic nervous system in children with attention-deficit/hyperactivity disorder (ADHD). Journal of Abnormal Child Psychology, 39, 841–852.
go back to reference Musser, E. D., Hawkey, E., Kachan‐Liu, S. S., Lees, P., Roullet, J. B., Goddard, K., ... & Nigg, J. T. (2014). Shared familial transmission of autism spectrum and attention‐deficit/hyperactivity disorders. Journal of Child Psychology and Psychiatry, 55, 819–827. Musser, E. D., Hawkey, E., Kachan‐Liu, S. S., Lees, P., Roullet, J. B., Goddard, K., ... & Nigg, J. T. (2014). Shared familial transmission of autism spectrum and attention‐deficit/hyperactivity disorders. Journal of Child Psychology and Psychiatry, 55, 819–827.
go back to reference Negrao, B. L., Bipath, P., van der Westhuizen, D., & Viljoen, M. (2011). Autonomic correlates at rest and during evoked attention in children with attention-deficit/hyperactivity disorder and effects of methylphenidate. Neuropsychobiology, 63(2), 82–91. doi:10.1159/00031754.CrossRefPubMed Negrao, B. L., Bipath, P., van der Westhuizen, D., & Viljoen, M. (2011). Autonomic correlates at rest and during evoked attention in children with attention-deficit/hyperactivity disorder and effects of methylphenidate. Neuropsychobiology, 63(2), 82–91. doi:10.​1159/​00031754.CrossRefPubMed
go back to reference Nigg, J. T. (2012). Future directions in ADHD etiology research. Journal of Clinical Child & Adolescent Psychology, 41, 524–533.CrossRef Nigg, J. T. (2012). Future directions in ADHD etiology research. Journal of Clinical Child & Adolescent Psychology, 41, 524–533.CrossRef
go back to reference Nigg, J. T., & Casey, B. J. (2005). An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neurosciences. Development and Psychopathology, 17, 785–806. doi:10.1017/S0954579405050376.PubMed Nigg, J. T., & Casey, B. J. (2005). An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neurosciences. Development and Psychopathology, 17, 785–806. doi:10.​1017/​S095457940505037​6.PubMed
go back to reference Porges, S. W. (2001). The Polyvagal Theory: phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146.CrossRefPubMed Porges, S. W. (2001). The Polyvagal Theory: phylogenetic substrates of a social nervous system. International Journal of Psychophysiology, 42, 123–146.CrossRefPubMed
go back to reference Raiker, J. S., Rapport, M. D., Kofler, M. J., & Sarver, D. E. (2012). Objectively-measured impulsivity and attention-deficit/hyperactivity disorder (ADHD): testing competing predictions from the working memory and behavioral inhibition models of ADHD. Journal of Abnormal Child Psychology, 40, 699–713.CrossRefPubMed Raiker, J. S., Rapport, M. D., Kofler, M. J., & Sarver, D. E. (2012). Objectively-measured impulsivity and attention-deficit/hyperactivity disorder (ADHD): testing competing predictions from the working memory and behavioral inhibition models of ADHD. Journal of Abnormal Child Psychology, 40, 699–713.CrossRefPubMed
go back to reference Rapport, M. D., Chung, K. M., Shore, G., & Isaacs, P. (2001). A conceptual model of child psychopathology: implications for understanding attention deficit hyperactivity disorder and treatment efficacy. Journal of Clinical Child Psychology, 30, 48–58.CrossRefPubMed Rapport, M. D., Chung, K. M., Shore, G., & Isaacs, P. (2001). A conceptual model of child psychopathology: implications for understanding attention deficit hyperactivity disorder and treatment efficacy. Journal of Clinical Child Psychology, 30, 48–58.CrossRefPubMed
go back to reference Rapport, M. D., Alderson, R. M., Kofler, M. J., Sarver, D. E., Bolden, J., & Sims, V. (2008). Working memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): the contribution of central executive and subsystem processes. Journal of Abnormal Child Psychology, 36, 825–837.CrossRefPubMed Rapport, M. D., Alderson, R. M., Kofler, M. J., Sarver, D. E., Bolden, J., & Sims, V. (2008). Working memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): the contribution of central executive and subsystem processes. Journal of Abnormal Child Psychology, 36, 825–837.CrossRefPubMed
go back to reference Rash, J. A., & Aguirre-Camacho, A. (2012). Attention-deficit hyperactivity disorder and cardiac vagal control: a systematic review. ADHD Attention Deficit and Hyperactivity Disorders, 4, 167–177.CrossRefPubMed Rash, J. A., & Aguirre-Camacho, A. (2012). Attention-deficit hyperactivity disorder and cardiac vagal control: a systematic review. ADHD Attention Deficit and Hyperactivity Disorders, 4, 167–177.CrossRefPubMed
go back to reference Sonuga-Barke, E. J. (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biological Psychiatry, 57, 1231–1238.CrossRefPubMed Sonuga-Barke, E. J. (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biological Psychiatry, 57, 1231–1238.CrossRefPubMed
go back to reference Sonuga-Barke, E. J., Dalen, L., & Remington, B. (2003). Do executive deficits and delay aversion make independent contributions to preschool attention-Deficit/Hyperactivity disorder symptoms? Journal of the American Academy of Child & Adolescent Psychiatry, 42, 1335.CrossRef Sonuga-Barke, E. J., Dalen, L., & Remington, B. (2003). Do executive deficits and delay aversion make independent contributions to preschool attention-Deficit/Hyperactivity disorder symptoms? Journal of the American Academy of Child & Adolescent Psychiatry, 42, 1335.CrossRef
go back to reference Thayer, J. F., Hansen, A. L., Saus-Rose, E., & Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Annals of Behavioral Medicine, 37, 141–153.CrossRefPubMed Thayer, J. F., Hansen, A. L., Saus-Rose, E., & Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Annals of Behavioral Medicine, 37, 141–153.CrossRefPubMed
go back to reference Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory. Cognitive, Affective, & Behavioral Neuroscience, 3, 255–274.CrossRef Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory. Cognitive, Affective, & Behavioral Neuroscience, 3, 255–274.CrossRef
go back to reference Wechsler, D. (2003). Wechsler intelligence scale for children–Fourth Edition (WISC-IV). San Antonio: The Psychological Corporation. Wechsler, D. (2003). Wechsler intelligence scale for children–Fourth Edition (WISC-IV). San Antonio: The Psychological Corporation.
go back to reference Willcutt, E. G., Nigg, J. T., Pennington, B. F., Solanto, M. V., Rohde, L. A., Tannock, R., … & Lahey, B. B. (2012). Validity of DSM-IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. Journal of Abnormal Psychology, 121, 991. Willcutt, E. G., Nigg, J. T., Pennington, B. F., Solanto, M. V., Rohde, L. A., Tannock, R., … & Lahey, B. B. (2012). Validity of DSM-IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. Journal of Abnormal Psychology, 121, 991.
Metagegevens
Titel
Variation in Parasympathetic Dysregulation Moderates Short-term Memory Problems in Childhood Attention-Deficit/Hyperactivity Disorder
Auteurs
Anthony R. Ward
Gabriela Alarcón
Joel T. Nigg
Erica D. Musser
Publicatiedatum
29-07-2015
Uitgeverij
Springer US
Gepubliceerd in
Research on Child and Adolescent Psychopathology / Uitgave 8/2015
Print ISSN: 2730-7166
Elektronisch ISSN: 2730-7174
DOI
https://doi.org/10.1007/s10802-015-0054-3

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