Differences in dual-task performance and prefrontal cortex activation between younger and older adults

BMC Neuroscience

Eric B Schneider³  Kenta Shigemori²  Shohei Ohgi¹  Hironori Ohsugi¹ 

[1] Graduate School of Health Sciences, Seirei Christopher University, 3453 Mikatahara-Cho, Hamamatsu-City, Shizuoka, 433-8558, Japan;Department of healthcare, Kansai University of Health and welfare science, 3-11-1, Asahigaoka, Kashiwara-City, Osaka, 582-0026, Japan;Johns Hopkins School of Medicine, Center for Surgical Trials and Outcomes Research, 600 N. Wolfe St, Baltimore, MD, 21205, USA

关键词: Attentional function;    Executive function;    Near-infrared spectroscopy;    Dual-task;   

Others  :  1140530
DOI  :  10.1186/1471-2202-14-10

 received in 2012-07-14, accepted in 2012-11-29,  发布年份 2013

【 摘 要 】

Background

The purpose of this study was to examine task-related changes in prefrontal cortex (PFC) activity during a dual-task in both healthy young and older adults and compare patterns of activation between the age groups. We also sought to determine whether brain activation during a dual-task relates to executive/attentional function and how measured factors associated with both of these functions vary between older and younger adults.

Results

Thirty-five healthy volunteers (20 young and 15 elderly) participated in this study. Near-infrared spectroscopy (NIRS) was employed to measure PFC activation during a single-task (performing calculations or stepping) and dual-task (performing both single-tasks at once). Cognitive function was assessed in the older patients with the Trail-making test part B (TMT-B). Major outcomes were task performance, brain activation during task (oxygenated haemoglobin: Oxy-Hb) measured by NIRS, and TMT-B score. Mixed ANOVAs were used to compare task factors and age groups in task performance. Mixed ANOVAs also compared task factors, age group and time factors in task-induced changes in measured Oxy-Hb. Among the older participants, correlations between the TMT-B score and Oxy-Hb values measured in each single-task and in the dual-task were examined using a Pearson correlation coefficient.

Oxy-Hb values were significantly increased in both the calculation task and the dual-task within patients in both age groups. However, the Oxy-Hb values associated with there were higher in the older group during the post-task period for the dual-task. Also, there were significant negative correlations between both task-performance accuracy and Oxy-Hb values during the dual-task and participant TMT-B scores.

Conclusions

Older adults demonstrated age-specific PFC activation in response to dual-task challenge. There was also a significant negative correlation between PFC activation during dual-task and executive/attentional function. These findings suggest that the high cognitive load induced by dual-task activity generates increased PFC activity in older adults. However, this relationship appeared to be strongest in participants with better baseline attention and executive functions.

【 授权许可】

   
2013 Ohsugi et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Ardila A, Ostrosky-Solis F, Rosselli M, Gómez C: Age-related cognitive decline during normal aging: the complex effect of education. Arch Clin Neuropsychol 2000, 15:495-513.
• [2]O’Sullivan M, Jones D, Summers P, Morris R, Williams S, Markus H: Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology 2000, 57:632-638.
• [3]lzheimer's Disease International: World Alzheimer Report 2010 The Global Economic Impact of Dementia. London; 2010.
• [4]Smith E, Jonides J: Storage and executive processes in the frontal lobes. Science 1999, 283:1657-1661.
• [5]Gray JR, Braver TS, Raichle ME: Integration of emotion and cognition in the lateral prefrontal cortex. Proc Natl Acad Sci U S A. 2002, 99:4115-4120.
• [6]Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD: The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 2000, 41:49-100.
• [7]West RL: An application of prefrontal cortex function theory to cognitive aging. Psychol Bull 1996, 120:272-292.
• [8]Fuster JM: The prefrontal cortex. 4th edition. London: Academic Press; 2008.
• [9]Scarmeas N, Stern Y: Cognitive reserve: implications for diagnosis and prevention of alzheimer’s disease. Curr Neurol Neurosci Rep 2004, 4:374-378.
• [10]Kawashima R, Okita K, Yamazaki R, Tajima N, Yoshida H, Taira M, Iwata K, Sasaki T, Maeyama K, Usui N, Sugimoto K: Reading aloud and arithmetic calculation improve frontal function of people with dementia. J Gerontol A Biol Sci Med Sci 2005, 60:380-384.
• [11]Jueptner M, Weiller C: Review: does measurement of regional cerebral blood flow reflect synaptic activity? implications for PET and fMRI. Neuroimage 1995, 2:148-156.
• [12]Kato T, Kamei A, Takashima S, Ozaki T: Human visual cortical function during photic stimulation monitoring by means of near-infrared spectroscopy. J Cereb Blood Flow Metab 1993, 13:516-520.
• [13]Nishijima T, Piriz J, Duflot S, Fernandez AM, Gaitan G, Gomez-Pinedo U, Verdugo JM, Leroy F, Soya H, Nuñez A, Torres-Aleman I: Neuronal activity drives localized blood–brain-barrier transport of serum insulin-like growth factor-I into the CNS. Neuron 2010, 67:834-846.
• [14]Ball K, Berch DB, Helmers KF, Jobe JB, Leveck MD, Marsiske M, Morris JN, Rebok GW, Smith DM, Tennstedt SL, Unverzagt FW, Willis SL: Advanced cognitive training for independent and vital elderly study group. Effects of cognitive training interventions with older adults: a randomized controlled trial. JAMA 2002, 288:2271-2281.
• [15]Clare L, Wilson BA, Carter G, Hodges JR: Cognitive rehabilitation as a component of early intervention in alzheimer’s disease: a single case study. Aging Ment Health 2003, 7:15-21.
• [16]Edwards JD, Wadley VG, Vance DE, Wood K, Roenker DL, Ball KK: The impact of speed of processing training on cognitive and everyday performance. Aging Ment Health 2005, 9:262-271.
• [17]Angevaren M, Aufdemkampe G, Verhaar HJ, Aleman A, Vanhees L: Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008, 16:CD005381.
• [18]Williams CL, Tappen RM: Exercise training for depressed older adults with alzheimer’s disease. Aging Ment Health 2008, 12:72-80.
• [19]Della Sala S, Baddeley A, Papagno C, Spinnler H: Dual-task paradigm: a means to examine the central executive. Ann N Y Acad Sci 1995, 769:161-171.
• [20]Silsupadol P, Shumway-Cook A, Lugade V, van Donkelaar P, Chou LS, Mayr U, Woollacott MH: Effects of single-task versus dual-task training on balance performance in older adults: a double-blind, randomized controlled trial. Arch Phys Med Rehabil 2009, 90:381-387.
• [21]Baddeley A: Working memory: looking back and looking forward. Nat Rev Neurosci 2003, 4:829-839.
• [22]Klingberg T: Limitations in information processing in the human brain: neuroimaging of dual task performance and working memory tasks. Prog Brain Res 2000, 126:195-102.
• [23]Stelzel C, Brandt SA, Schubert T: Neural mechanisms of concurrent stimulus processing in dual tasks. Neuroimage 2009, 48:237-248.
• [24]Pedroso R, Coelho F, Santos-Galduróz R, Costa J, Gobbi S, Stella F: Balance, executive functions and falls in elderly with alzheimer’s disease (AD): a longitudinal study. Arch Gerontol Geriatr 2012, 54:348-351.
• [25]Schwenk M, Zieschang T, Oster P, Hauer K: Dual-task performances can be improved in patients with dementia: a randomized controlled trial. Neurology 2010, 74:1961-1968.
• [26]Erickson KI, Colcombe SJ, Wadhwa R, Bherer L, Peterson MS, Scalf PE, Kim JS, Alvarado M, Kramer AF: Training-induced plasticity in older adults: effects of training on hemispheric asymmetry. Neurobiol Aging 2007, 28:272-283.
• [27]D’Esposito M, Detre J, Alsop D, Shin R, Atlas S, Grossman M: The neural basis of the central executive system of working memory. Nature 1995, 378:279-281.
• [28]Koechlin E, Basso G, Pietrini P, Panzer S, Grafman J: The role of the anterior prefrontal cortex in human cognition. Nature 1999, 399:148-151.
• [29]Callicott JH, Mattay VS, Bertolino A, Finn K, Coppola R, Frank JA, Goldberg TE, Weinberger DR: Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cereb Cortex 1999, 9:20-26.
• [30]Reuter-Lorenz P, Cappell K: Neurocognitive aging and the compensation hypothesis. Curr Dir Psychol Sci 2008, 17:177-182.
• [31]Schroeter ML, Zysset S, Kruggel F, von Cramon DY: Age dependency of hemodynamic response as measured by functional near-infrared spectroscopy. NeuroImage 2003, 19:555-564.
• [32]Okada E, Firbank M, Schweiger M, Arridge SR, Cope M, Delpy DT: Theoretical and experimental investigation of near-infrared light propagation in a model of the adult head. Appl Opt 1997, 36:21-31.
• [33]Tamura M, Hoshi Y, Okada F: Localized near-infrared spectroscopy and functional optical imaging of brain activity. Philos Trans R Soc Lond B Biol Sci 1997, 352:737-742.
• [34]Hoshi Y, Kobayashi N, Tamura M: Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. J Appl Physiol 2001, 90:1657-1662.
• [35]Honda N, Matuoka T, Sawada Y, Nakano N, Suwen L, Higashimoto Y, Fukuda K, Ohgi S, Kato A: Reorganization of sensorimotor function after functional hemispherectomy studied using near-infrared spectroscopy. Pediatr Neurosurg 2010, 46:313-317.
• [36]Shigemori K, Ohgi S, Okuyama E, Shimura T, Schneider E: The factorial structure of the mini-mental state examination (MMSE) in Japanese dementia patients. BMC Geriatr 2010, 10:36. BioMed Central Full Text
• [37]Folstein M: Mini-mental and son. Int J Geriatr Psychiatry 1998, 13:290-294.
• [38]Kortte KB, Horner MD, Windham WK: The trail making test, part B: cognitive flexibility or ability to maintain set? Appl Neuropsychol 2002, 9:106-109.
• [39]Stuss DT, Levine B: Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol 2002, 53:401-433.
• [40]Zakzanis KK, Mraz R, Graham SJ: An fMRI study of the trail making test. Neuropsychologia 2005, 43:1878-1886.
• [41]Ashendorf L, Jefferson A, O’Connor M, Chaisson C, Green R, Stern R: Trail making test errors in normal aging, mild cognitive impairment, and dementia. Arch Clin Neuropsychol 2008, 23:129-137.
• [42]Bland JM, Altman DG: Multiple significance tests: the bonferroni method. BMJ 1995, 310:170.
• [43]Herbster AN, Mintun MA, Nebes RD, Becker JT: Regional cerebral blood flow during word and nonword reading. Hum Brain Mapp 1997, 5:84-92.
• [44]Rueckert L, Lange N, Partiot A, Appollonio I, Litvan I, Le Bihan D, Grafman J: Visualizing cortical activation during mental calculation with functional MRI. Neuroimage 1996, 3:97-103.
• [45]Raz N, Gunning FM, Head D, Dupuis JH, McQuain J, Briggs SD, Loken WJ, Thornton AE, Acker JD: Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb Cortex 1997, 7:268-282.
• [46]Imran MB, Kawashima R, Awata S, Sato K, Kinomura S, Ono S, Yoshioka S, Sato M, Fukuda H: Parametric mapping of cerebral blood flow deficits in alzheimer’s disease: a SPECT study using HMPAO and image standardization technique. J Nucl Med 1999, 40:244-249.
• [47]Montero-Odasso M, Bergman H, Phillips NA, Wong CH, Sourial N, Chertkow H: Dual-tasking and gait in people with mild cognitive impairment. The effect of working memory. BMC Geriatr 2009, 9:41. BioMed Central Full Text
• [48]Richter MM, Herrmann MJ, Ehlis AC, Plichta MM, Fallgatter AJ: Brain activation in elderly people with and without dementia: influences of gender and medication. World J Biol Psychiatry 2007, 8:23-29.