Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T16:23:15.142Z Has data issue: false hasContentIssue false

Age Differences in Reaction Times and a Neurophysiological Marker of Cholinergic Activity

Published online by Cambridge University Press:  02 November 2015

Marielle Young-Bernier*
Affiliation:
School of Psychology, University of Ottawa Bruyère Research Institute, University of Ottawa
Annick N. Tanguay
Affiliation:
School of Psychology, University of Ottawa Bruyère Research Institute, University of Ottawa
François Tremblay
Affiliation:
School of Psychology, University of Ottawa Bruyère Research Institute, University of Ottawa School of Rehabilitation Sciences, University of Ottawa Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, University of Ottawa
Patrick S. R. Davidson*
Affiliation:
School of Psychology, University of Ottawa Bruyère Research Institute, University of Ottawa Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, University of Ottawa
*
La correspondance et les demandes de tirés-à-part doivent être adressées à: / Correspondence and requests for offprints should be sent to: Marielle Young-Bernier, PhD School of Psychology University of Ottawa 136 Jean-Jacques Lussier Ottawa, ON K1N 6N5 ([email protected]) or Patrick Davidson, PhD School of Psychology University of Ottawa 136 Jean-Jacques Lussier Ottawa, ON K1N 6N5 ([email protected])
La correspondance et les demandes de tirés-à-part doivent être adressées à: / Correspondence and requests for offprints should be sent to: Marielle Young-Bernier, PhD School of Psychology University of Ottawa 136 Jean-Jacques Lussier Ottawa, ON K1N 6N5 ([email protected]) or Patrick Davidson, PhD School of Psychology University of Ottawa 136 Jean-Jacques Lussier Ottawa, ON K1N 6N5 ([email protected])

Abstract

The deterioration of the cholinergic system in aging is hypothesized to contribute to age-related declines in attention. We investigated potential age differences in performance on the Attention Network Test (ANT) and intra-individual variability in speed (RT-IIV) on go/no-go and choice reaction time tasks in young and healthy older adults. We also asked whether short-latency afferent inhibition (SAI), a neurophysiological marker of central cholinergic activity obtained via transcranial magnetic stimulation, might be correlated with performance. Older adults were slower on the ANT and exhibited greater RT-IIV than young adults on the multiple choice RT task, but there were no age differences on the ANT network scores (alerting, orienting, and executive control). SAI was diminished in older adults, but it was not significantly correlated with performance. It may only be in cases of severe cholinergic dysfunction that relations with attention emerge. Other brain mechanisms may also be stronger predictors of functions relating to attention.

Résumé

La détérioration du système cholinergique lors du vieillissement normal semble contribuer au déclin de l’attention avec l’âge. Nous avons examiné l’effet potentiel de l’âge sur la performance au « Attention Network Test » (ANT) ainsi que sur la variabilité intra-individuelle dans la vitesse des réponses à une tâche go/no-go et à une tâche de temps de réaction (TR) à choix multiples chez un groupe de jeunes adultes et de personnes âgées en santé. Nous avons ensuite examiné si un marqueur neurophysiologique de l’activité cholinergique dérivé de la stimulation magnétique transcrânienne (i.e., inhibition afférente à courte latence; IACL) était associé à la performance. Les personnes âgées montraient un ralentissement au ANT ainsi qu’une plus grande variabilité intra-individuelle que les jeunes adultes à la tâche de TR à choix multiples, mais il n’y avait pas de différence liée à l’âge dans les scores reflétant les réseaux attentionnels du ANT (vigilance, orientation aux stimuli et contrôle exécutif). Les niveaux de IACL étaient diminués chez les personnes âgées, mais ils n’étaient pas associés à la performance. Il est possible que des relations entre le marqueur de l’activité cholinergique et l’attention émergent seulement en cas de déficits de neurotransmission sévères. D’autres mécanismes corticaux pourraient aussi être plus fortement associés aux fonctions liées à l’attention.

Type
Articles
Copyright
Copyright © Canadian Association on Gerontology 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

Awiszus, F. (2003). TMS and threshold hunting. Supplements to Clinical Neurophysiology, 56, 1323. doi: 10.1016/S1567-424X(09)70205-3.Google Scholar
Backman, L., Nyberg, L., Lindenberger, U., Li, S. C., & Farde, L. (2006). The correlative triad among aging, dopamine, and cognition: current status and future prospects. Neuroscience & Biobehavioral Reviews, 30(6), 791807. doi: 10.1016/j.neubiorev.2006.06.005.Google Scholar
Davidson, M. C., & Marrocco, R. T. (2000). Local infusion of scopolamine into intraparietal cortex slows covert orienting in rhesus monkeys. Journal of Neurophysiology, 83(3), 15361549.Google Scholar
Di Lazzaro, V., Oliviero, A., Profice, P., Pennisi, M. A., Di Giovanni, S., & Zito, G. (2000). Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Experimental Brain Research, 135(4), 455461. doi: 10.1007/s002210000543.Google Scholar
Di Lazzaro, V., Oliviero, A., Tonali, P. A., Marra, C., Daniele, A., & Profice, P. (2002). Noninvasive in vivo assessment of cholinergic cortical circuits in AD using transcranial magnetic stimulation. Neurology, 59(3), 392397.Google Scholar
Duchek, J. M., Balota, D. A., Tse, C. S., Holtzman, D. M., Fagan, A. M., & Goate, A. M. (2009). The utility of intraindividual variability in selective attention tasks as an early marker for Alzheimer’s disease. Neuropsychology, 23(6), 746758. doi: 10.1037/a0016583.Google Scholar
Dumas, J. A., & Newhouse, P. A. (2011). The cholinergic hypothesis of cognitive aging revisited again: Cholinergic functional compensation. Pharmacology Biochemistry and Behavior, 99(2), 254261. doi: 10.1016/j.pbb.2011.02.022.Google Scholar
Duzel, S., Munte, T. F., Lindenberger, U., Bunzeck, N., Schutze, H., & Heinze, H. J. (2010). Basal forebrain integrity and cognitive memory profile in healthy aging. Brain Research, 1308, 124136. doi: 10.1016/j.brainres.2009.10.048.Google Scholar
Dykiert, D., Der, G., Starr, J. M., & Deary, I. J. (2012). Age differences in intra-individual variability in simple and choice reaction time: Systematic review and meta-analysis. PLoS One, 7(10), e45759. doi: 10.1371/journal.pone.0045759.Google Scholar
Fan, J., McCandliss, B. D., Fossella, J., Flombaum, J. I., & Posner, M. I. (2005). The activation of attentional networks. NeuroImage, 26(2), 471479. doi: 10.1016/j.neuroimage.2005.02.004.Google Scholar
Fan, J., McCandliss, B. D., Sommer, T., Raz, A., & Posner, M. I. (2002). Testing the efficiency and independence of attentional networks. Journal of Cognitive Neuroscience, 14(3), 340347. doi: 10.1162/089892902317361886.CrossRefGoogle ScholarPubMed
Faul, F., Erdfelder, E., Lang, A. G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175191. doi: 10.3758/BF03193146.CrossRefGoogle ScholarPubMed
Fernandez, P. J., Campoy, G., Garcia Santos, J. M., Antequera, M. M., Garcia-Sevilla, J., & Castillo, A. (2011). Is there a specific pattern of attention deficit in mild cognitive impairment with subcortical vascular features? Evidence from the Attention Network Test. Dementia and Geriatric Cognitive Disorders, 31(4), 268275. doi: 10.1159/000327165.CrossRefGoogle Scholar
Fernandez-Duque, D., & Black, S. E. (2006). Attentional networks in normal aging and Alzheimer’s disease. Neuropsychology, 20(2), 133143. doi: 10.1037/0894-4105.20.2.133.CrossRefGoogle ScholarPubMed
Finkel, D., & McGue, M. (2007). Genetic and environmental influences on intraindividual variability in reaction time. Experimental Aging Research, 33(1), 1335. doi: 10.1080/03610730601006222.CrossRefGoogle ScholarPubMed
Furey, M. L. (2011). The prominent role of stimulus processing: Cholinergic function and dysfunction in cognition. Current Opinion in Neurology, 24(4), 364370. doi: 10.1097/WCO.0b013e328348bda5.Google Scholar
Gamboz, N., Zamarian, S., & Cavallero, C. (2010). Age-related differences in the attention network test (ANT). Experimental Aging Research, 36(3), 287305. doi: 10.1080/0361073X.2010.484729.CrossRefGoogle ScholarPubMed
Grothe, M., Heinsen, H., & Teipel, S. J. (2012). Atrophy of the cholinergic Basal forebrain over the adult age range and in early stages of Alzheimer’s disease. Biological Psychiatry, 71(9), 805813. doi: 10.1016/j.biopsych.2011.06.019.Google Scholar
Hasselmo, M. E., & Sarter, M. (2011). Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology, 36(1), 5273. doi: 10.1038/npp.2010.104.CrossRefGoogle ScholarPubMed
Hultsch, D. F., MacDonald, S. W., & Dixon, R. A. (2002). Variability in reaction time performance of younger and older adults. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 57(2), P101115. doi: 10.1093/geronb/57.2.P101.Google Scholar
Ishigami, Y., & Klein, R. M. (2010). Repeated measurement of the components of attention using two versions of the Attention Network Test (ANT): Stability, isolability, robustness, and reliability. Journal of Neuroscience Methods, 190(1), 117128. doi: 10.1016/j.jneumeth.2010.04.019.Google Scholar
Jennings, J. M., Dagenbach, D., Engle, C. M., & Funke, L. J. (2007). Age-related changes and the attention network task: An examination of alerting, orienting, and executive function. Neuropsychology, Development, and Cognition Section B, Aging, Neuropsychology and Cognition , 14(4), 353 369 . doi: 10.1080/13825580600788837 . Google Scholar
Kleykamp, B. A., Jennings, J. M., Blank, M. D., & Eissenberg, T. (2005). The effects of nicotine on attention and working memory in never-smokers. Psychology of Addictive Behaviors, 19(4), 433438. doi: 10.1037/0893-164X.19.4.433.CrossRefGoogle ScholarPubMed
Knight, M., & Mather, M. (2013). Look out – It’s your off-peak time of day! Time of day matters more for alerting than for orienting or executive attention. Experimental Aging Research, 39(3), 305321. doi: 10.1080/0361073X.2013.779197.CrossRefGoogle ScholarPubMed
Lackner, C. L., Bowman, L. C., & Sabbagh, M. A. (2010). Dopaminergic functioning and preschoolers’ theory of mind. Neuropsychologia, 48(6), 17671774. doi: 10.1016/j.neuropsychologia.2010.02.027.Google Scholar
MacDonald, S. W., Li, S. C., & Backman, L. (2009). Neural underpinnings of within-person variability in cognitive functioning. Psychology and Aging, 24(4), 792808. doi: 10.1037/a0017798.Google Scholar
MacDonald, S. W., Nyberg, L., & Backman, L. (2006). Intra-individual variability in behavior: Links to brain structure, neurotransmission and neuronal activity. Trends in Neuroscience, 29(8), 474480. doi: 10.1016/j.tins.2006.06.011.Google Scholar
Macleod, J. W., Lawrence, M. A., McConnell, M. M., Eskes, G. A., Klein, R. M., & Shore, D. I. (2010). Appraising the ANT: Psychometric and theoretical considerations of the Attention Network Test. Neuropsychology, 24(5), 637651. doi: 10.1037/a0019803.CrossRefGoogle ScholarPubMed
Mahoney, J. R., Verghese, J., Goldin, Y., Lipton, R., & Holtzer, R. (2010). Alerting, orienting, and executive attention in older adults. Journal of the International Neuropsychological Society, 16(5), 877889. doi: 10.1017/S1355617710000767.Google Scholar
Martella, D., Manzanares, S., Campoy, G., Roca, J., Antunez, C., & Fuentes, L. J. (2014). Phasic and tonic alerting in mild cognitive impairment: A preliminary study. Experimental Gerontology, 49, 3539. doi: 10.1016/j.exger.2013.11.001.Google Scholar
Nardone, R., Bergmann, J., Christova, M., Caleri, F., Tezzon, F., & Ladurner, G. (2012). Short latency afferent inhibition differs among the subtypes of mild cognitive impairment. Journal of Neural Transmission, 119(4), 463471. doi: 10.1007/s00702-011-0725-3.Google Scholar
Nasreddine, Z. S., Phillips, N. A., Bedirian, V., Charbonneau, S., Whitehead, V., & Collin, I. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695699. doi: 10.1111/j.1532-5415.2005.53221.x.Google Scholar
Petersen, S. E., & Posner, M. I. (2012). The attention system of the human brain: 20 years after. Annual Review of Neuroscience, 35, 7389. doi: 10.1146/annurev-neuro-062111-150525.Google Scholar
Phillips, M., Rogers, P., Haworth, J., Bayer, A., & Tales, A. (2013). Intra-individual reaction time variability in mild cognitive impairment and Alzheimer’s disease: Gender, processing load and speed factors. PLoS One, 8(6), e65712. doi: 10.1371/journal.pone.0065712.Google Scholar
Robbins, T. W., Semple, J., Kumar, R., Truman, M. I., Shorter, J., & Ferraro, A. (1997). Effects of scopolamine on delayed-matching-to-sample and paired associates tests of visual memory and learning in human subjects: Comparison with diazepam and implications for dementia. Psychopharmacology, 134(1), 95106. doi: 10.1007/s002130050430.Google Scholar
Rossetti, H. C., Lacritz, L. H., Cullum, C. M., & Weiner, M. F. (2011). Normative data for the Montreal Cognitive Assessment (MoCA) in a population-based sample. Neurology, 77(13), 12721275. doi: 10.1212/WNL.0b013e318230208a.Google Scholar
Sarter, M., Hasselmo, M. E., Bruno, J. P., & Givens, B. (2005). Unraveling the attentional functions of cortical cholinergic inputs: Interactions between signal-driven and cognitive modulation of signal detection. Brain Research Reviews, 48(1), 98111. doi: 10.1016/j.brainresrev.2004.08.006.Google Scholar
Sarter, M., & Turchi, J. (2002). Age- and dementia-associated impairments in divided attention: Psychological constructs, animal models, and underlying neuronal mechanisms. Dementia and Geriatric Cognitive Disorders, 13(1), 4658. doi: 10.1159/000048633.Google Scholar
Schliebs, R., & Arendt, T. (2006). The significance of the cholinergic system in the brain during aging and in Alzheimer’s disease. Journal of Neural Transmission, 113(11), 16251644. doi: 10.1007/s00702-006-0579-2.Google Scholar
Thienel, R., Kellermann, T., Schall, U., Voss, B., Reske, M., & Halfter, S. (2009). Muscarinic antagonist effects on executive control of attention. International Journal of Neuropsychopharmacology, 12(10), 13071317. doi: 10.1017/S146114570999068X.CrossRefGoogle ScholarPubMed
Thienel, R., Voss, B., Kellermann, T., Reske, M., Halfter, S., & Sheldrick, A. J. (2009). Nicotinic antagonist effects on functional attention networks. International Journal of Neuropsychopharmacology, 12(10), 12951305. doi: 10.1017/S1461145709990551.Google Scholar
Tokimura, H., Di Lazzaro, V., Tokimura, Y., Oliviero, A., Profice, P., & Insola, A. (2000). Short latency inhibition of human hand motor cortex by somatosensory input from the hand. The Journal of Physiology, 523 Pt 2, 503513.Google Scholar
Van Dam, N. T., Sano, M., Mitsis, E. M., Grossman, H. T., Gu, X., & Park, Y. (2013). Functional neural correlates of attentional deficits in amnestic mild cognitive impairment. PLoS One, 8(1), e54035. doi: 10.1371/journal.pone.0054035.Google Scholar
Wang, Y. F., Cui, Q., Liu, F., Huo, Y. J., Lu, F. M., & Chen, H. (2014). A new method for computing attention network scores and relationships between attention networks. PLoS One, 9(3), e89733. doi: 10.1371/journal.pone.0089733.Google Scholar
Westlye, L. T., Grydeland, H., Walhovd, K. B., & Fjell, A. M. (2011). Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cerebral Cortex, 21(2), 345356. doi: 10.1093/cercor/bhq101.Google Scholar
Wignall, N. D., & de Wit, H. (2011). Effects of nicotine on attention and inhibitory control in healthy nonsmokers. Experimental and Clinical Psychopharmacology, 19(3), 183191. doi: 10.1037/a0023292.Google Scholar
Young-Bernier, M., Davidson, P. S., & Tremblay, F. (2012). Paired-pulse afferent modulation of TMS responses reveals a selective decrease in short latency afferent inhibition with age. Neurobiology of Aging, 33(4), 835 e831–811. doi: 10.1016/j.neurobiolaging.2011.08.012.Google Scholar
Young-Bernier, M., Kamil, Y., Tremblay, F., & Davidson, P.S. (2012). Associations between a neurophysiological marker of central cholinergic activity and cognitive functions in young and older adults. Behavioral and Brain Functions, 8, 17. doi: 10.1186/1744-9081-8-17.Google Scholar
Zhou, S. S., Fan, J., Lee, T. M., Wang, C. Q., & Wang, K. (2011). Age-related differences in attentional networks of alerting and executive control in young, middle-aged, and older Chinese adults. Brain and Cognition, 75(2), 205210. doi: 10.1016/j.bandc.2010.12.003.Google Scholar