Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-28T06:28:19.936Z Has data issue: false hasContentIssue false
  • English
  • Français

Association between Salivary Alpha-Amylase and Executive Functioning in Healthy Children

Published online by Cambridge University Press:  14 May 2019

Enrique F. Maldonado Open the ORCID record for Enrique F. Maldonado [Opens in a new window] ,
Mari Nislin ,
Laura Marín ,
Ana Martín-Escribano ,
Alfredo Enguix ,
Cristina López ,
Alba Magarín ,
Ana Álamo ,
Paula Ortíz  and
Marina Muñoz
...Show all authors
Enrique F. Maldonado*
Affiliation:
Universidad de Málaga (Spain)
Mari Nislin
Affiliation:
The Education University of Hong Kong (China)
Laura Marín
Affiliation:
Hospital Universitario Virgen de la Victoria, Málaga (Spain)
Ana Martín-Escribano
Affiliation:
Hospital Universitario Virgen de la Victoria, Málaga (Spain)
Alfredo Enguix
Affiliation:
Hospital Universitario Virgen de la Victoria, Málaga (Spain)
Cristina López
Affiliation:
Universidad de Málaga (Spain)
Alba Magarín
Affiliation:
Universidad de Málaga (Spain)
Ana Álamo
Affiliation:
Universidad de Málaga (Spain)
Paula Ortíz
Affiliation:
Universidad de Málaga (Spain)
Marina Muñoz
Affiliation:
Universidad de Málaga (Spain)
Silvia García
Affiliation:
Universidad de Málaga (Spain)
*
*Correspondence concerning this article should be addressed to Enrique F. Maldonado. Universidad de Málaga. Andalucía Tech, Facultad de Psicología, Departamento de Psicobiología y Metodología de las Ciencias del Comportamiento. Campus Teatinos. 29071 Málaga (Spain). E-mail: fcomm@uma.es
Get access Rights & Permissions [Opens in a new window]

Abstract

The main aim of this study was to confirm the relationship between executive performance and salivary alpha-amylase (SAA) activity in a sample of 64 healthy children (39 boys), and compare it to the association of SAA output and salivary flow rate (SFR). Executive functioning was assessed via fluency, trail-making, rings and inhibition tasks from the Batería de Evaluación Neuropsicológica de la Función Ejecutiva en Niños [Battery of Neuropsychological Assessment for Executive Function in Children] (ENFEN), merged into an ENFEN total score. SAA activity, output, and SFR were measured at baseline, one minute before, and one minute after the end of a neuropsychological testing session. Our results confirmed a direct, linear and significant association between SAA activity and executive functioning, r(64) = .351, p < .05, and extended it to SAA output, r(64) =.431, p < .05. The mean level of SAA output was the best predictor of executive functioning (β = .431, p < .05) and explained 18.2 % of the variance in ENFEN total score. In sum, and compared to SAA activity, measuring SAA output may be a more precise and indirect marker to assess executive functioning in children.

Keywords

alpha-amylasechildrenENFENexecutive functioningsaliva
Type
Research Article
Information
The Spanish Journal of Psychology , Volume 22 , 2019 , E24
Copyright
Copyright © Universidad Complutense de Madrid and Colegio Oficial de Psicólogos de Madrid 2019 

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.)

Footnotes

We would like to acknowledge the parents and teachers of the children of the Pintor Revello de Toro and Cayetano Bolivar primary schools who participated in our study.

How to cite this article:

Maldonado, E. F., Nislin, M., Marín, L., Martín-Escribano, A., Enguix, A., López, C., … García, S. (2019). Association between salivary alpha-amylase and executive functioning in healthy children. The Spanish Journal of Psychology, 22. e24. Doi:10.1017/sjp.2019.26

References

Ardila, A. (2013). Development of metacognitive and emotional executive functions in children. Applied Neuropsychology: Child, 2, 82–87. http://doi.org/10.1080/21622965.2013.748388CrossRefGoogle ScholarPubMed
Arhakis, A., Karagiannis, V., & Kalfas, S. (2013). Salivary alpha-amylase activity and salivary flow rate in young adults. The Open Dentistry Journal, 7, 7–15. http://doi.org/10.2174/1874210601307010007CrossRefGoogle ScholarPubMed
Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450. http://doi.org/10.1146/annurev.neuro.28.061604.135709CrossRefGoogle ScholarPubMed
Berry, D., Blair, C., Willoughby, M., Granger, D. A., & Family Life Project Key Investigators (2012). Salivary alpha-amylase and cortisol in infancy and toddlerhood: Direct and indirect relations with executive functioning and academic ability in childhood. Psychoneuroendocrinology, 37, 1700–1711. http://doi.org/10.1016/j.psyneuen.2012.03.002CrossRefGoogle Scholar
Berry, D., Blair, C., Ursache, A., Willoughby, M. T., Granger, D. A., & Family Life Project Key Investigators. (2014). Early childcare, executive functioning, and the moderating role of early stress physiology. Developmental Psychopathology, 50, 1250–1261. http://doi.org/10.1037/a0034700Google Scholar
Berthelsen, D., Hayes, N., White, S. L. J., & Williams, K. E. (2017). Executive function in adolescence: Associations with child and family risk factors and self-regulation in early childhood. Frontiers in Psychology, 8. http://doi.org/10.3389/fpsyg.2017.00903CrossRefGoogle ScholarPubMed
Blair, C. (2010). Stress and the development of self-regulation in context. Child Development Perspectives, 4, 181–188. http://doi.org/10.1111/j.1750-8606.2010.00145.xCrossRefGoogle ScholarPubMed
Blair, C., & Raver, C. C. (2014). Closing the achievement gap through modification of neurocognitive and neuroendocrine function: Results from a cluster randomized controlled trial of an innovative approach to the education of children in kindergarten. PLOS ONE, 9, e112393. http://doi.org/10.1371/journal.pone.0112393CrossRefGoogle ScholarPubMed
Blair, C., & Raver, C. C. (2016). Poverty, stress, and brain development: New directions for prevention and intervention. Academic Pediatrics, 16, S30–S36. http://doi.org/10.1016/j.acap.2016.01.010CrossRefGoogle ScholarPubMed
Blair, C., Ursache, A., Greenberg, M., Vernon-Feagans, L., & Family Life Project Investigators (2015). Multiple aspects of self-regulation uniquely predict mathematics but not letter-word knowledge in the early elementary grades. Developmental Psychopathology, 51, 459–472. http://doi.org/10.1037/a0038813Google Scholar
Bodrova, E., & Leong, D. J. (2007). Tools of the mind: The Vygotskian approach to early childhood education. New York, NY: Merrill/Prentice Hall.Google Scholar
Congdon, E. & Canli, T. (2005). The endophenotype of impulsivity: Reaching consilience through behavioral, genetic, and neuroimaging approaches. Behavioral and Cognitive Neuroscience Reviews, 4, 262–281. http://doi.org/10.1177/1534582305285980CrossRefGoogle ScholarPubMed
Ditzen, B., Ehlert, U., & Nater, U. M. (2014). Associations between salivary alpha-amylase and catecholamines-a multilevel modeling approach. Biological Psychology, 103, 15–18. http://doi.org/10.1016/j.biopsycho.2014.08.001CrossRefGoogle Scholar
Ehlert, U., Erni, K., Hebisch, G., & Nater, U. (2006). Salivary alpha-amylase levels after yohimbine challenge in healthy men. The Journal of Clinical Endocrinology and Metabolism, 91, 5130–5133. http://doi.org/10.1210/jc.2006-0461CrossRefGoogle ScholarPubMed
Ekström, J., Murakami, M., Inzitari, R., Khosravani, N., Fanali, C., Cabras, T., ... Castagnola, M. (2009). RP-HPLC-ESI-MS characterization of novel peptide fragments related to rat parotid secretory protein in parasympathetic induced saliva. Journal of Separation Science, 32(17), 2944–2952. http://doi.org/10.1002/jssc.200900197CrossRefGoogle ScholarPubMed
Kirschbaum, C., & Hellhammer, D. H. (1989). Salivary cortisol in psychobiological research: An overview. Neuropsychobiology, 22, 150–169. http://doi.org/10.1159/000118611CrossRefGoogle ScholarPubMed
Kuebler, U., von Känel, R., Heimgartner, N., Zuccarella-Hackl, C., Stirnimann, G., Ehlert, U., & Wirtz, P. H. (2014). Norepinephrine infusion with and without alpha-adrenergic blockade by phentolamine increases salivary alpha amylase in healthy men. Psychoneuroendocrinology, 49, 290–298. http://doi.org/10.1016/j.psyneuen.2014.07.023CrossRefGoogle ScholarPubMed
Nagy, T., van Lien, R., Willemsen, G., Proctor, G., Efting, M., Fülöp, M., ... Bosch, J. A. (2015). A fluid response: Alpha-amylase reactions to acute laboratory stress are related to sample timing and saliva flow rate. Biological Psychology, 109, 111–119. http://doi.org/10.1016/j.biopsycho.2015.04.012CrossRefGoogle ScholarPubMed
Nater, U. M., & Rohleder, N. (2009). Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: Current state of research. Psychoneuroendocrinology, 34, 486–496. http://doi.org/10.1016/j.psyneuen.2009.01.014CrossRefGoogle Scholar
Nicolaides, N. C., Kyratzi, E., Lamprokostopoulou, A., Chrousos, G. P., & Charmandari, E. (2015). Stress, the stress system and the role of glucocorticoids. NeuroImmunoModulation, 22, 6–19. http://doi.org/10.1159/000362736CrossRefGoogle ScholarPubMed
Nielsen, S. E., & Mather, M. (2016). Comparison of two isometric handgrip protocols on sympathetic arousal in women. Physiology & Behavior, 142, 5–13. http://doi.org/10.1016/j.physbeh.2015.01.031CrossRefGoogle Scholar
Noordermeer, S. D., Luman, M., & Oosterlaan, J. (2016). A systematic review and meta-analysis of neuroimaging in oppositional defiant disorder (ODD) and conduct disorder (CD) taking attention-deficit hyperactivity disorder (ADHD) into account. Neuropsychology Review, 26, 44–72. http://doi.org/10.1007/s11065-015-9315-8CrossRefGoogle Scholar
Ocklenburg, S., Beste, C., Arning, L., Peterburs, J., & Güntürkün, O. (2014). The ontogenesis of language lateralization and its relation to handedness. Neuroscience & Biobehavioral Reviews, 43, 191–198. http://doi.org/10.1016/j.neubiorev.2014.04.008CrossRefGoogle ScholarPubMed
Portellano, J. A. (2009). ENFEN. Evaluación neuropsicológica de las funciones ejecutivas en niños [Neuropsychological assessment of executive functions in children]. Madrid, Spain: Editorial TEA.Google Scholar
Ramos, B. P., & Arnsten, A. F. (2007). Adrenergic pharmacology and cognition: Focus on prefrontal cortex. Pharmacology & Therapeutics, 113, 523–536. http://doi.org/10.1016/j.pharmthera.2006.11.006CrossRefGoogle ScholarPubMed
Robbins, T. W., & Arnsten, A. F. (2009). The neuropsychopharmacology of fronto-executive function: Monamingergic modulation. Annual Review of Neuroscience, 32, 267–287. http://doi.org/10.1146/annurev.neuro.051508.135535CrossRefGoogle ScholarPubMed
Rohleder, N., & Nater, U. M. (2009). Determinants of salivary alpha-amylase in humans and methodological considerations. Psychoneuroendocrinology, 34, 469–485. http://doi.org/10.1016/j.psyneuen.2008.12.004CrossRefGoogle ScholarPubMed
Sánchez-Navarro, J. P., Maldonado, E. F., Martínez-Selva, J. M., Enguix, A., & Ortiz, C., (2012). Salivary alpha-amylase changes promoted by sustained exposure to affective pictures. Psychophysiology, 49, 1601–1609. http://doi.org/10.1111/j.1469-8986.2012.01475.xCrossRefGoogle ScholarPubMed
Sapolsky, R. M. (2000). Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Archives of General Psychiatry, 57, 925–935. http://doi.org/10.1001/archpsyc.57.10.925CrossRefGoogle ScholarPubMed
Schumacher, S., Kirschbaum, C., Fydrich, T., & Ströhle, A. (2013). Is salivary alpha-amylase an indicator of autonomic nervous system dysregulations in mental disorders? A review of preliminary findings and the interactions with cortisol. Psychoneuroendocrinology, 38, 729–743. http://doi.org/10.1016/j.psyneuen.2013.02.003CrossRefGoogle ScholarPubMed
Sibille, E., & French, B. (2013). Biological substrates underpinning diagnosis of major depression. The International Journal of Neuropsychopharmacology, 16, 1893–1909. http://doi.org/10.1017/S1461145713000436CrossRefGoogle ScholarPubMed
Skeide, M. A., & Friederici, A. D. (2016). The ontogeny of the cortical language network. Nature Reviews Neuroscience, 17, 323–332. http://doi.org/10.1038/nrn.2016.23CrossRefGoogle ScholarPubMed
Stavrou, S., Nicolaides, N. C., Critselis, E., Darviri, C., Charmandari, E., & Chrousos, G. P. (2017). Paediatric stress: From neuroendocrinology to contemporary disorders. European Journal of Clinical Investigation, 47, 262–269. http://doi.org/10.1111/eci.12724CrossRefGoogle ScholarPubMed
Ursache, A., & Noble, K. G. (2016). Neurocognitive development in socioeconomic context: Multiple mechanisms and implications for measuring socioeconomic status. Psychophysiology, 53, 71–82. http://doi.org/10.1111/psyp.12547CrossRefGoogle ScholarPubMed
van Leusden, J. W., Sellaro, R., & Colzato, L. S. (2015). Transcutaneous vagal nerve stimulation (tVNS): A new neuromodulation tool in healthy humans? Frontiers in Psychology, 6, 102. http://doi.org/10.3389/fpsyg.2015.00102CrossRefGoogle ScholarPubMed
van Stegeren, A. Rohleder, N., Everaerd, W., & Wolf, O. T. (2006). Salivary alpha amylase as marker for adrenergic activity during stress: Effect of betablockade. Psychoneuroendocrinology, 31, 137–141. http://doi.org/10.1016/j.psyneuen.2005.05.012CrossRefGoogle ScholarPubMed
Warren, C. M., van den Brink, R. L., Nieuwenhuis, S., & Bosch, J. A. (2017). Norepinephrine transporter blocker atomoxetine increases salivary alpha amylase. Psychoneuroendocrinology, 78, 233–236. http://doi.org/10.1016/j.psyneuen.2017.01.029CrossRefGoogle ScholarPubMed
Weymar, M., Ventura-Bort, C., Genheimer, H., Wirkner, J., Wendt, J., & Hamm, A. (2017). The P300 and the LC-NE system: New insights from transcutaneous vagus nerve stimulation (TVNS). Psychophysiology, 54(Suppl. 1), 145.Google Scholar
Willemen, A. M., Koot, H. M., Ferdinand, R. F., Goossens, F. A., & Schuengel, C. (2008). Change in psychopathology in referred children: the role of life events and perceived stress. Journal of Child Psychology and Psychiatry, 49(11), 1175–1183. http://doi.org/10.1111/j.1469-7610.2008.01925.xGoogle ScholarPubMed
Willoughby, M. T., Blair, C. B., Wirth, R. J., & Greenberg, M. (2010). The measurement of executive function at age 3 years: Psychometric properties and criterion validity of a new battery of tasks. Psychological Assessment, 22, 306–317. http://doi.org/10.1037/a0018708CrossRefGoogle ScholarPubMed
Zelazo, P. D., & Müller, U. (2002). Executive function in typical and atypical development. In Goswami, U. (Ed.), Handbook of childhood cognitive development (pp. 445–469). Oxford, UK: Blackwell.CrossRefGoogle Scholar