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Published in: Dysphagia 3/2010

01-09-2010 | Original Article

Age-Related Differences in Laterality of Cortical Activations in Swallowing

Authors: Georgia A. Malandraki, Bradley P. Sutton, Adrienne L. Perlman, Dimitrios C. Karampinos

Published in: Dysphagia | Issue 3/2010

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Abstract

The present study examined age differences in neural lateralization patterns during swallowing and three related tasks, using functional magnetic resonance imaging (fMRI). Ten healthy right-handed young adults (mean age = 21.7 years, SD = 2.1 years) and nine healthy elders (mean age = 70.2 years, SD = 3.9 years) were scanned in a 3-T MRI head scanner. Participants were visually cued to “prepare to swallow,” “swallow,” “tap your tongue,” and “clear your throat” in randomized order. Laterality preference for each task was examined within and between groups using region-of-interest (ROI) analyses in seven areas of the left and right primary sensorimotor and premotor cortices. Results of the within-group comparisons verified a more active role of the left premotor cortex in motor-cognitive planning of deglutition in both young and older adults and a more active role of selected areas of the right hemisphere during swallowing in young adults. Greater variability was seen during tongue tapping and throat clearing in both groups. Finally, as people age the cortical hemispheric control of swallowing seems to start becoming more symmetrical/bilateral, which may indicate neural compensatory mechanisms of the aging brain commonly seen for other motor and cognitive functions.
Literature
1.
go back to reference Robbins J, Levine RL. Swallowing after unilateral stroke of the cerebral cortex: preliminary experience. Dysphagia. 1988;3(1):11–7.CrossRefPubMed Robbins J, Levine RL. Swallowing after unilateral stroke of the cerebral cortex: preliminary experience. Dysphagia. 1988;3(1):11–7.CrossRefPubMed
2.
go back to reference Robbins J, Levine RL, Maser A, Rosenbek JC, Kempster GB. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993;74:1295–300.CrossRefPubMed Robbins J, Levine RL, Maser A, Rosenbek JC, Kempster GB. Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993;74:1295–300.CrossRefPubMed
3.
go back to reference Daniels SK, Foundas AL, Iglesia G, Sullivan M. Lesion site in unilateral stroke patients with dysphagia. J Stroke Cerebr Dis. 1996;6(1):30–4.CrossRef Daniels SK, Foundas AL, Iglesia G, Sullivan M. Lesion site in unilateral stroke patients with dysphagia. J Stroke Cerebr Dis. 1996;6(1):30–4.CrossRef
4.
go back to reference Daniels SK, Corey DM, Fraychinaud A, DePolo A, Foundas AL. Swallowing lateralization: the effects of modified dual-task interference. Dysphagia. 2006;21(1):21–7.CrossRefPubMed Daniels SK, Corey DM, Fraychinaud A, DePolo A, Foundas AL. Swallowing lateralization: the effects of modified dual-task interference. Dysphagia. 2006;21(1):21–7.CrossRefPubMed
5.
go back to reference Alberts MJ, Horner J, Gray L, Brazer SR. Aspiration after stroke: lesion analysis by brain MRI. Dysphagia. 1992;7:170–3.CrossRefPubMed Alberts MJ, Horner J, Gray L, Brazer SR. Aspiration after stroke: lesion analysis by brain MRI. Dysphagia. 1992;7:170–3.CrossRefPubMed
6.
go back to reference Daniels SK, Foundas AL. Lesion localization in acute stroke patients with risk of aspiration. J Neuroimaging. 1999;9:91–7.PubMed Daniels SK, Foundas AL. Lesion localization in acute stroke patients with risk of aspiration. J Neuroimaging. 1999;9:91–7.PubMed
7.
go back to reference Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9:90–5.CrossRefPubMed Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9:90–5.CrossRefPubMed
8.
go back to reference Daniels SK, Brailey K, Foundas AL. Lingual discoordination and dysphagia following acute stroke: analyses of lesion localization. Dysphagia. 1999;14:85–92.CrossRefPubMed Daniels SK, Brailey K, Foundas AL. Lingual discoordination and dysphagia following acute stroke: analyses of lesion localization. Dysphagia. 1999;14:85–92.CrossRefPubMed
9.
go back to reference Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S, et al. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999;277:G219–25.PubMed Hamdy S, Mikulis DJ, Crawley A, Xue S, Lau H, Henry S, et al. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999;277:G219–25.PubMed
10.
go back to reference Mosier KM, Liu WC, Maldjian JA, Shah R, Modi B. Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol. 1999;20:1520–6.PubMed Mosier KM, Liu WC, Maldjian JA, Shah R, Modi B. Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol. 1999;20:1520–6.PubMed
11.
go back to reference Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85:938–50.PubMed Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85:938–50.PubMed
12.
go back to reference Watanabe J, Suguira M, Miura N, Watanabe Y, Maeda Y, Matsue Y, et al. The human parietal cortex is involved in spatial processing of tongue movement—an fMRI study. NeuroImage. 2004;21:1289–99.CrossRefPubMed Watanabe J, Suguira M, Miura N, Watanabe Y, Maeda Y, Matsue Y, et al. The human parietal cortex is involved in spatial processing of tongue movement—an fMRI study. NeuroImage. 2004;21:1289–99.CrossRefPubMed
13.
go back to reference Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H2 15O PET activation. J Neurophysiol. 1999;81:1917–26.PubMed Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H2 15O PET activation. J Neurophysiol. 1999;81:1917–26.PubMed
14.
go back to reference Hutchinson S, Kobayashi M, Horkan CM, Pascual-Leone A, Alexander MP, Schlaug G. Age-related differences in movement representation. NeuroImage. 2002;17:1720–8.CrossRefPubMed Hutchinson S, Kobayashi M, Horkan CM, Pascual-Leone A, Alexander MP, Schlaug G. Age-related differences in movement representation. NeuroImage. 2002;17:1720–8.CrossRefPubMed
15.
go back to reference Mattay VS, Fera F, Tessitore A, Hariri AR, Das S, Callicott JH, et al. Neurophysiological correlates of age-related changes in human motor function. Neurology. 2002;58:630–5.PubMed Mattay VS, Fera F, Tessitore A, Hariri AR, Das S, Callicott JH, et al. Neurophysiological correlates of age-related changes in human motor function. Neurology. 2002;58:630–5.PubMed
16.
go back to reference Sailer A, Dichgans J, Gerloff C. The influence of normal aging on the cortical processing of a simple motor task. Neurology. 2000;55:979–85.PubMed Sailer A, Dichgans J, Gerloff C. The influence of normal aging on the cortical processing of a simple motor task. Neurology. 2000;55:979–85.PubMed
17.
go back to reference Riecker A, Groschel K, Ackermann H, Steinbrink C, Witte O, Kastrup A. Functional significance of age-related differences in motor activation patterns. NeuroImage. 2006;32(3):1345–54.CrossRefPubMed Riecker A, Groschel K, Ackermann H, Steinbrink C, Witte O, Kastrup A. Functional significance of age-related differences in motor activation patterns. NeuroImage. 2006;32(3):1345–54.CrossRefPubMed
18.
go back to reference Huettel SA, Singerman JD, McCarthy G. The effects of aging upon the hemodynamic response measured by functional MRI. NeuroImage. 2001;13:161–75.CrossRefPubMed Huettel SA, Singerman JD, McCarthy G. The effects of aging upon the hemodynamic response measured by functional MRI. NeuroImage. 2001;13:161–75.CrossRefPubMed
19.
go back to reference Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC. Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. NeuroImage. 2006;32(3):1250–6.CrossRefPubMed Naccarato M, Calautti C, Jones PS, Day DJ, Carpenter TA, Baron JC. Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study. NeuroImage. 2006;32(3):1250–6.CrossRefPubMed
20.
go back to reference Reuter-Lorenz P, Jonides J, Smith ES, Hartley A, Miller A, Marshuetz C, et al. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci. 2000;12:174–87.CrossRefPubMed Reuter-Lorenz P, Jonides J, Smith ES, Hartley A, Miller A, Marshuetz C, et al. Age differences in the frontal lateralization of verbal and spatial working memory revealed by PET. J Cogn Neurosci. 2000;12:174–87.CrossRefPubMed
21.
go back to reference Cao Y, Vikingstad EM, Paige George K, Johnson AF, Welch KMA. Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke. 1999;30:2331–40.PubMed Cao Y, Vikingstad EM, Paige George K, Johnson AF, Welch KMA. Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke. 1999;30:2331–40.PubMed
22.
go back to reference Silvestrini M, Cupini LM, Placidi F, Diomedi M, Bernardi G. Bilateral hemispheric activation in the early recovery of motor function after stroke. Stroke. 1998;29:1305–10.PubMed Silvestrini M, Cupini LM, Placidi F, Diomedi M, Bernardi G. Bilateral hemispheric activation in the early recovery of motor function after stroke. Stroke. 1998;29:1305–10.PubMed
23.
go back to reference Buckner RL. Age-related changes in neural activity during episodic memory. Paper presented at the Symposium on Neuroscience, Aging & Cognition, San Francisco; 2002. Buckner RL. Age-related changes in neural activity during episodic memory. Paper presented at the Symposium on Neuroscience, Aging & Cognition, San Francisco; 2002.
24.
go back to reference Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRefPubMed Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRefPubMed
25.
go back to reference Gracco VL, Tremblay P, Pike B. Imaging speech production using fMRI. NeuroImage. 2005;26(1):294–301.CrossRefPubMed Gracco VL, Tremblay P, Pike B. Imaging speech production using fMRI. NeuroImage. 2005;26(1):294–301.CrossRefPubMed
26.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825–41.CrossRefPubMed Jenkinson M, Bannister P, Brady M, Smith S. Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825–41.CrossRefPubMed
28.
go back to reference Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280:G354–60.PubMed Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280:G354–60.PubMed
29.
go back to reference Kern MK, Birn R, Jaradeh S, Jesmanowicz A, Cox R, Hyde J, et al. Swallow-related cerebral cortical activity maps are not specific to deglutition. Am J Physiol Gastrointest Liver Physiol. 2001;280:G531–8.PubMed Kern MK, Birn R, Jaradeh S, Jesmanowicz A, Cox R, Hyde J, et al. Swallow-related cerebral cortical activity maps are not specific to deglutition. Am J Physiol Gastrointest Liver Physiol. 2001;280:G531–8.PubMed
30.
go back to reference Martin RE, MacIntosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS, et al. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92:2428–43.CrossRefPubMed Martin RE, MacIntosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS, et al. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92:2428–43.CrossRefPubMed
31.
go back to reference Martin RE, Barr A, MacIntosh B, Smith R, Stevens T, Taves D, et al. Cerebral cortical processing of swallowing in older adults. Exp Brain Res. 2007;176:12–22.CrossRefPubMed Martin RE, Barr A, MacIntosh B, Smith R, Stevens T, Taves D, et al. Cerebral cortical processing of swallowing in older adults. Exp Brain Res. 2007;176:12–22.CrossRefPubMed
32.
go back to reference Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140:280–9.CrossRefPubMed Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001;140:280–9.CrossRefPubMed
33.
go back to reference Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of the cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18:71–7.CrossRefPubMed Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of the cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18:71–7.CrossRefPubMed
34.
go back to reference Toogood JA, Barr AM, Stevens TK, Gati JS, Menon RS, Martin RE. Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study. Exp Brain Res. 2005;161(1):81–90.CrossRefPubMed Toogood JA, Barr AM, Stevens TK, Gati JS, Menon RS, Martin RE. Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study. Exp Brain Res. 2005;161(1):81–90.CrossRefPubMed
35.
go back to reference Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, et al. Two different areas within the primary motor cortex of man. Nature. 1996;382:805–7.CrossRefPubMed Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, et al. Two different areas within the primary motor cortex of man. Nature. 1996;382:805–7.CrossRefPubMed
36.
go back to reference Geyer S, Schleicher A, Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. NeuroImage. 1999;10:63–83.CrossRefPubMed Geyer S, Schleicher A, Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. NeuroImage. 1999;10:63–83.CrossRefPubMed
37.
go back to reference Geyer S, Schormann T, Mohlberg H, Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. Part 2. Spatial normalization to standard anatomical space. NeuroImage. 2000;11:684–96.CrossRefPubMed Geyer S, Schormann T, Mohlberg H, Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. Part 2. Spatial normalization to standard anatomical space. NeuroImage. 2000;11:684–96.CrossRefPubMed
38.
go back to reference Grefkes C, Geyer S, Schormann T, Roland P, Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage. 2001;14:617–31.CrossRefPubMed Grefkes C, Geyer S, Schormann T, Roland P, Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage. 2001;14:617–31.CrossRefPubMed
39.
go back to reference Geyer S. The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Adv Anat Embryol Cell Biol. 2004;174(I–VIII):1–89. Geyer S. The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Adv Anat Embryol Cell Biol. 2004;174(I–VIII):1–89.
40.
go back to reference Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage. 2005;25:1325–35.CrossRefPubMed Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage. 2005;25:1325–35.CrossRefPubMed
41.
go back to reference Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, Hughes DG, et al. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2(11):1217–24.CrossRefPubMed Hamdy S, Aziz Q, Rothwell JC, Singh KD, Barlow J, Hughes DG, et al. The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996;2(11):1217–24.CrossRefPubMed
42.
go back to reference Dziewas R, Soros P, Ishii R, Chau W, Henningsen H, Ringelstein EB, et al. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. NeuroImage. 2003;20:135–44.CrossRefPubMed Dziewas R, Soros P, Ishii R, Chau W, Henningsen H, Ringelstein EB, et al. Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. NeuroImage. 2003;20:135–44.CrossRefPubMed
43.
go back to reference Pardo JV, Wood TD, Costello PA, Pardo PJ, Lee JT. PET study of the localization and laterality of lingual somatosensory processing in humans. Neurosci Lett. 1997;243:2–26. Pardo JV, Wood TD, Costello PA, Pardo PJ, Lee JT. PET study of the localization and laterality of lingual somatosensory processing in humans. Neurosci Lett. 1997;243:2–26.
44.
go back to reference Corfield DR, Murphy K, Josephs O, Fink GR, Frackowiak RSJ, Guz A, et al. Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. J Appl Physiol. 1999;86(5):1468–77.PubMed Corfield DR, Murphy K, Josephs O, Fink GR, Frackowiak RSJ, Guz A, et al. Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. J Appl Physiol. 1999;86(5):1468–77.PubMed
45.
go back to reference Pineiro R, Pendlebury S, Johansen-Berg H, Matthews PM. Functional MRI detects posterior shifts in primary sensorimotor cortex after stroke: evidence for adaptive reorganization? Stroke. 2001;32:1134–9.PubMed Pineiro R, Pendlebury S, Johansen-Berg H, Matthews PM. Functional MRI detects posterior shifts in primary sensorimotor cortex after stroke: evidence for adaptive reorganization? Stroke. 2001;32:1134–9.PubMed
46.
go back to reference Gur RC, Gunning-Dixon FM, Turetsky BI, Bilker WB, Gur RE. Brain region and sex differences in age association with brain volume: a quantitative MRI study of healthy young adults. Am J Geriatr Psychiatry. 2002;10(1):72–80.PubMed Gur RC, Gunning-Dixon FM, Turetsky BI, Bilker WB, Gur RE. Brain region and sex differences in age association with brain volume: a quantitative MRI study of healthy young adults. Am J Geriatr Psychiatry. 2002;10(1):72–80.PubMed
47.
go back to reference Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp 2009. doi: 10.1002/hbm.20743. Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp 2009. doi: 10.​1002/​hbm.​20743.
Metadata
Title
Age-Related Differences in Laterality of Cortical Activations in Swallowing
Authors
Georgia A. Malandraki
Bradley P. Sutton
Adrienne L. Perlman
Dimitrios C. Karampinos
Publication date
01-09-2010
Publisher
Springer-Verlag
Published in
Dysphagia / Issue 3/2010
Print ISSN: 0179-051X
Electronic ISSN: 1432-0460
DOI
https://doi.org/10.1007/s00455-009-9250-z

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