Sains Malaysiana 44(9)(2015): 1339–1350

Kesan Penuaan ke atas Kehubungan Berkesan Otak semasa Pemprosesan Ingatan Bekerja daripada Perspektif Pemodelan Sebab dan Akibat Dinamik

(The Effect of Ageing on Brain Effective Connectivity during Working Memory Processing

from the Perspective of Dynamic Causal Modelling)

HANANI ABDUL MANAN^1,2, AHMAD NAZLIM YUSOFF^1* & SITI ZAMRATOL-MAI SARAH MUKARI³

¹Program Pengimejan Diagnostik & Radioterapi, Pusat Pengajian Sains Diagnostik dan Kesihatan Gunaan, Fakulti Sains Kesihatan, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz

50300 Kuala Lumpur, Wilayah Persekutuan, Malaysia

²Pusat Perkhidmatan dan Penyelidikan Neurosains (P3NEURO), Kampus Kesihatan, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan Darul Naim, Malaysia

³Program Audiologi, Pusat Pengajian Sains Rehabilitasi, Fakulti Sains Kesihatan, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Wilayah Persekutuan

Malaysia

Diserahkan: 8 Januari 2015/Diterima: 25 Mei 2015

ABSTRAK

Proses penuaan seringkali dikaitkan dengan kemerosotan sistem kognitif. Kemerosotan tersebut bermula seawal usia dua puluhan dan berterusan secara linear. Walau bagaimanapun, kesan penuaan ke atas ciri kehubungan antara kawasan otak masih belum difahami. Dalam kajian ini, pengimejan resonans magnet kefungsian (fMRI) digunakan untuk mengkaji kesan penuaan ke atas kehubungan otak yang terhasil daripada tugasan mengulang secara terbalik (BRT). Subjek normal dalam empat kumpulan umur iaitu 20-29 tahun (n=14), 30-39 tahun (n=14), 40-49 tahun (n=10) dan 50-65 tahun (n=14) mengambil bahagian dalam kajian ini. Stimulus BRT terdiri daripada satu siri lima perkataan yang diberi secara auditori. Pemetaan statistik berparameter (SPM) dan pemodelan sebab dan akibat dinamik (DCM) digunakan untuk menentukan pengaktifan dan kehubungan otak. Sebanyak 200 model kehubungan intrahemisfera dan 150 interhemisfera dibina bagi menguji kewujudan gandingan antara girus temporal superior (STG), girus Heschl (HG), talamus (TH) dan girus presentral (PCG) kesemua subjek. Keputusan DCM menunjukkan subjek keempat-empat kumpulan umur menggunakan kehubungan intrahemisfera yang sama semasa tugasan BRT. Kehubungan interhemisfera pula didapati berubah menjadi semakin kompleks apabila usia meningkat. Perubahan tersebut didapati bermula pada usia 40 tahun. Keputusan ini menyokong penemuan terdahulu bahawa penuaan menyebabkan perubahan pada sistem neuron otak seterusnya mempengaruhi pemprosesan kognitif.

Kata kunci: DCM; fungsi eksekutif pusat; fMRI; kehubungan efektif; pemprosesan auditori; penuaan

ABSTRACT

Ageing process is often associated with cognitive system declination. The decline begins as early as in the twenties and continues linearly. However, the effects of ageing on connectivity charactersistics between the brain areas have yet to be understood. In the present study, functional magnetic resonance imaging (fMRI) was used to investigate the effects of ageing on brain connectivity resulting from the backward repeat task (BRT). Normal participants with four age groups which were 20-29 years (n=14), 30-39 years (n=14), 40-49 years (n=10) and 50-65 years (n=14) participated in this study. The BRT stimulus consisted of a series of five words given auditorily. Statistical parametric mapping (SPM) and dynamic causal modeling (DCM) was used to determine brain activation and connectivity. Two-hundred intrahemispheric and 150 interhemispheric connectivity models were constructed to test the existence of coupling between superior temporal gyrus (STG), Heschl’s gyrus (HG), thalamus (TH) and precentral gyrus (PCG) on all subjects. DCM results showed that participants from the four age groups used the same intrahemispheric connectivity during BRT task. The interhemipheric connectivity changed and became more complex with ageing. The change was found to start at the age of 40. This result supports previous finding that ageing causes changes in the brain neuronal system and consequently affects cognitive processing.

Keywords: Ageing; auditory processing; central executive function; DCM; effective connectivity; fMRI

RUJUKAN

Abdul Manan, H., Yusoff, A.N., Franz, E.A. & Sarah Mukari, S.Z. 2013. Early and late shift of brain laterality in STG, HG, and cerebellum with normal aging during a short-term memory task. ISRN Neurol 2013: 892072.

Alexander, M.P., Gillingham, S., Schweizer, T. & Stuss, D.T. 2012. Cognitive impairments due to focal cerebellar injuries in adults. Cortex 48(8): 980-990.

Baddeley, A. 2003a. Working memory and language: An overview. J. Commun. Disord. 36(3): 189-208.

Baddeley, A. 2003b. Working memory: Looking back and looking forward. Nat. Rev. Neurosci. 4(10): 829-839.

Baddeley, A. 2000. The episodic buffer: A new component of working memory? Trends Cogn. Sci. 4(11): 417-423.

Bayliss, D.M., Jarrold, C., Gunn, D.M. & Baddeley, A.D. 2003. The complexities of complex span: Explaining individual differences in working memory in children and adults. J. Exp. Psychol. Gen. 132(1): 71-92.

Brett, M., Johnsrude, I.S. & Owen, A.M. 2002. The problem of functional localization in the human brain. Nat. Rev. Neurosci. 3(3): 243-249.

Burton, M.W. & Small, S.L. 2006. Functional neuroanatomy of segmenting speech and nonspeech. Cortex 42(4): 644-651.

Cabeza, R. 2002. Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychol. Aging 17(1): 85-100.

Cabeza, R., Daselaar, S.M., Dolcos, F., Prince, S.E., Budde, M. & Nyberg, L. 2004. Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb Cortex 14(4): 364-375.

Cabeza, R., Dolcos, F., Prince, S.E., Rice, H.J., Weissman, D.H. & Nyberg, L. 2003. Attention-related activity during episodic memory retrieval: A cross-function fMRI study. Neuropsychologia 41(3): 390-399.

Cabeza, R., Anderson, N.D., Locantore, J.K. & McIntosh, A.R. 2002. Aging gracefully: Compensatory brain activity in high-performing older adults. Neuroimage 17(3): 1394-1402.

Choi, H.J., Lee, D.Y., Seo, E.H., Jo, M.K., Sohn, B.K., Choe, Y.M., Byun, M.S., Kim, J.W., Kim, S.G., Yoon, J.C., Jhoo, J.H., Kim, K.W. & Woo, J.I. 2014. A normative study of the digit span in an educationally diverse elderly population. Psychiatry Investig. 11(1): 39-43.

Desmond, J.E. & Glover, G.H. 2002. Estimating sample size in functional MRI (fMRI) neuroimaging studies: Statistical power analyses. Journal of Neuroscience Methods 118: 115-128.

Dew, I.T., Buchler, N., Dobbins, I.G. & Cabeza, R. 2012. Where is ELSA? The early to late shift in aging. Cereb Cortex 22(11): 2542-2553.

Dolcos, F., Rice, H.J. & Cabeza, R. 2002. Hemispheric asymmetry and aging: Right hemisphere decline or asymmetry reduction. Neurosci. Biobehav. Rev. 26(7): 819-825.

Dos Santos Sequeira, S., Specht, K., Hamalainen, H. & Hugdahl, K. 2008. The effects of background noise on dichotic listening to consonant-vowel syllables. Brain Lang. 107(1): 11-15.

Eickhoff, S.B., Stephan, K.E., Mohlberg, H., Grefkes, C., Fink, G.R., Amunts, K. & Zilles, K. 2005. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25(4): 1325-1335.

Folstein, M.F., Folstein, S.E. & McHugh, P.R. 1975. Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12(3): 189-198.

Friston, K.J., Harrison, L. & Penny, W. 2003. Dynamic causal modelling. Neuroimage 19(4): 1273-1302.

Hall, D.A., Haggard, M.P., Akeroyd, M.A., Palmer, A.R., Summerfield, A.Q., Elliott, M.R., Gurney, E.M. & Bowtell, R.W. 1999. “Sparse” temporal sampling in auditory fMRI. Hum. Brain Mapp. 7(3): 213-223.

Hammers, A., Koepp, M.J., Free, S.L., Brett, M., Richardson, M.P., Labbe, C., Cunningham, V.J., Brooks, D.J. & Duncan, J. 2002. Implementation and application of a brain template for multiple volumes of interest. Hum. Brain Mapp. 15(3): 165-174.

Harding, I.H., Yücel, M., Harrison, B.J., Pantelis, C. & Breakspear, M. 2015. Effective connectivity within the frontoparietal control network differentiates cognitive control and working memory. Neuroimage 106(0): 144-153.

Heilbronner, R.L., Henry, G.K., Buck, P., Adams, R.L. & Fogle, T. 1991. Lateralized brain damage and performance on trail making A and B, digit span forward and backward, and TPT memory and location. Arch. Clin. Neuropsychol. 6(4): 251-258.

Ivanova, M.V. & Hallowell, B. 2014. A new modified listening span task to enhance validity of working memory assessment for people with and without aphasia. Journal of Communication Disorders 52(0): 78-98.

Maldjian, J.A., Laurienti, P.J., Kraft, R.A. & Burdette, J.H. 2003. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3): 1233-1239.

Manan, H.A., Franz, E.A., Yusoff, A.N. & Mukari, S.Z. 2015. The effects of aging on the brain activation pattern during a speech perception task: An fMRI study. Aging Clin Exp Res. 27(1): 27-36.

Manan, H.A., Franz, E.A., Yusoff, A.N. & Mukari, S.Z.M.S. 2013. Age-related laterality shifts in auditory and attention networks with normal ageing: Effects on a working memory task. Neurology Psychiatry and Brain Research 19(4): 180- 191.

Manan, H.A., Franz, E.A., Yusoff, A.N. & Mukari, S.Z.M. S. 2012. Hippocampal-cerebellar involvement in enhancement of performance in word-based BRT with the presence of background noise: An initial fMRI study. Psychology and Neuroscience 5(2): 247-256.

Matilainen, L.E., Talvitie, S.S., Pekkonen, E., Alku, P., May, P.J. & Tiitinen, H. 2010. The effects of healthy aging on auditory processing in humans as indexed by transient brain responses. Clin. Neurophysiol. 121(6): 902-911.

Mitchell, K.J., Johnson, M.K., Raye, C.L. & D’Esposito, M. 2000. fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. Brain Res. Cogn. Brain Res. 10(1-2): 197-206.

Oldfield, R.C. 1971. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9(1): 97-113.

Resnick, S.M., Goldszal, A.F., Davatzikos, C., Golski, S., Kraut, M.A., Metter, E.J., Bryan, R.N. & Zonderman, A.B. 2000. One-year age changes in MRI brain volumes in older adults. Cerebral Cortex 10(5): 464-472.

Reuter-Lorenz, P. 2002. New visions of the aging mind and brain. Trends Cogn. Sci. 6(9): 394.

Reuter-Lorenz, P.A., Jonides, J., Smith, E.E., Hartley, A., Miller, A., Marshuetz, C. & Koeppe, R.A. 2000. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J. Cogn. Neurosci. 12(1): 174-187.

St Jacques, P.L., Rubin, D.C. & Cabeza, R. 2012. Age-related effects on the neural correlates of autobiographical memory retrieval. Neurobiol. Aging 33(7): 1298-1310.

Stephan, K.E., Penny, W.D., Moran, R.J., den Ouden, H.E., Daunizeau, J. & Friston, K.J. 2010. Ten simple rules for dynamic causal modeling. Neuroimage 49(4): 3099-3109.

Stephan, K.E., Penny, W.D., Daunizeau, J., Moran, R.J. & Friston, K.J. 2009. Bayesian model selection for group studies. Neuroimage 46(4): 1004-1017.

Ting, S.K., Hameed, S., Tan, E.K., Gabriel, C. & Doshi, K. 2014. Digit span: A comparison of Chinese versus alphabetic language speakers in dysexecutive dementia patients. J. Neurol. Neurosurg. Psychiatry 85(1): 117-118.

Wilckens, K.A., Erickson, K.I. & Wheeler, M.E. 2012. Age-related decline in controlled retrieval: The role of the PFC and sleep. Neural Plast. 2012: 624795.

Yusoff, A.N., Manan, H.A., Mukari, S.Z.S., Hamid, K.A. & Franz, E.A. 2014. Brain activation and psychophysiologic interaction in association with a phonological working memory task. Modern Applied Science 8(5): 97-114.

Yusoff, A.N., Mohamad, M., Hamid, K.A., Abd Hamid, A.I. & Mukari, S.Z.M.S. 2011. Acquisition, analyses and interpretation of fMRI data: A study on the effective connectivity in human primary auditory cortices. Sains Malaysiana 40(6): 665-678.

*Pengarang untuk surat-menyurat; email: nazlimtrw@ukm.edu.my