Neural processing during older adults' comprehension of spoken sentences: Age differences in resource allocation and connectivity

Cerebral Cortex

Volumn 20, Issue 4, 2010, Pages 773-782

  Peelle, Jonathan E ^a,c   Troiani, Vanessa ^a   Wingfield, Arthur ^b   Grossman, Murray ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

Author keywords

Cognitive aging; fMRI; Language; Sentence processing; Speech

Indexed keywords

ACCURACY; ADULT; AGED; AGING; ARTICLE; BRAIN CORTEX; CINGULATE GYRUS; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NERVE CELL; NERVE CELL NETWORK; NORMAL HUMAN; OXYGEN BLOOD LEVEL; PARIETAL LOBE; PRIORITY JOURNAL; SPEECH RATE; VERBAL COMMUNICATION;

ADULT; AGE FACTORS; AGED; AGING; BRAIN MAPPING; CEREBRAL CORTEX; COMPREHENSION; FEMALE; FUNCTIONAL LATERALITY; GERIATRIC ASSESSMENT; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LANGUAGE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; NEURAL PATHWAYS; OXYGEN; SEX FACTORS; SPEECH;

EID: 77949358880     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp142     Document Type: Article

References (77)

1. Amici S, Brambati SM, Wilkins DP, Ogar J, Dronkers NL. 2007. Anatomical correlates of sentence comprehension and verbal working memory in neurodegenerative disease. J Neurosci. 27:6282-6290.
2. Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL. 2007. Disruption of large-scale brain systems in advanced aging. Neuron. 56:924-935.
3. Aron AR, Poldrack RA. 2006. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci. 26:2424-2433.
4. Ashburner J, Friston KJ. 1997. Multimodal image coregistration and partitioning- a unified framework. Neuroimage. 6:209-217.
5. Ashburner J, Friston KJ. 2005. Unified segmentation. Neuroimage. 26:839-851.
6. Awh E, Jonides J, Smith EE, Schumacher EH, Koeppe RA, Katz S. 1996. Dissociation of storage and rehearsal in verbal working memory: evidence from positron emission tomography. Psychol Sci. 7:25-31.
7. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET. 2000. Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex. 10:512-528.
8. Buchsbaum BR, Olsen RK, Koch P, Berman KF. 2005. Human dorsal and ventral auditory streams subserve rehearsal-based and echoic processes during verbal working memory. Neuron. 48:687-697.
9. Cabeza R. 2002. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging. 17:85-100.
10. Cabeza R, Anderson ND, Locantore JK, McIntosh AR. 2002. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage. 17:1394-1402.
11. Caplan D, Alpert N, Waters G. 1998. Effects of syntactic structure and propositional number on patterns of regional cerebral blood flow. J Cogn Neurosci. 10:541-552.
12. Caplan D, Alpert N, Waters G. 1999. PET studies of syntactic processing with auditory sentence presentation. Neuroimage. 9:343-351.
13. Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE. 1997. Temporal dynamics of brain activation during a working memory task. Nature. 386:604-608.
14. Cooke A, Zurif EB, DeVita C, Alsop D, Koenig P, Detre J, Gee J, Pinango M, Balogh J, Grossman M. 2002. Neural basis for sentence comprehension: grammatical and short-term memory components. Hum Brain Mapp. 15:80-94.
15. Crinion JT, Lambon Ralph MA, Warburton EA, Howard D, Wise RJS. 2003. Temporal lobe regions engaged during normal speech comprehension. Brain. 126:1193-1201.
16. Daselaar SM, Fleck MS, Dobbins IG, Madden DJ, Cabeza R. 2006. Effects of healthy aging on hippocampal and rhinal memory functions: an event-related fMRI study. Cereb Cortex. 16:1771-1782.
17. D'Esposito M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J. 1998. Functional MRI studies of spatial and nonspatial working memory. Cogn Brain Res. 7:1-13.
18. D'Esposito M, Postle BR, Rypma B. 2000. Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp Brain Res. 133:3-11.
19. Davis MH, Johnsrude IS. 2003. Hierarchical processing in spoken language comprehension. J Neurosci. 23:3423-3431.
20. Devlin JT, Matthews PM, Rushworth MFS. 2003. Semantic processing in the left inferior prefrontal cortex: a combined functional magnetic resonance imaging and transcranial magnetic stimulation study. J Cogn Neurosci. 15:71-84.
21. Duarte A, Henson RN, Graham KS. 2008. The effects of aging on the neural correlates of subjective and objective recollection. Cereb Cortex. 18:2169-2180.
22. Edmister WB, Talavage TM, Ledden PJ, Weisskoff RM. 1999. Improved auditory cortex imaging using clustered volume acquisitions. Hum Brain Mapp. 7:89-97.
23. Ferreira F, Henderson JM, Anes MD, Weeks PA, McFarlane DK. 1996. Effects of lexical frequency and syntactic complexity in spoken-language comprehension: evidence from the auditory moving-window technique. J Exp Psychol Learn Mem Cogn. 22:324-335.
24. Fiebach CJ, Schlesewsky M, Lohmann G, von Cramon DY, Friederici AD. 2005. Revisiting the role of Broca's area in sentence processing: syntactic integration versus syntactic working memory. Hum Brain Mapp. 24:79-91.
25. Friederici AD, Fiebach CJ, Schlesewsky M, Bornkessel ID, von Cramon DY. 2006. Processing linguistic complexity and grammaticality in the left frontal cortex. Cereb Cortex. 16:1709-1717.
26. Friederici AD, Ruschemeyer SA, Hahne A, Fiebach CJ. 2003. The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. Cereb Cortex. 13:170-177.
27. Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiak RSJ. 1995. Spatial registration and normalization of images. Hum Brain Mapp. 2:165-189.
28. Grady CL, McIntosh AR, Craik FIM. 2003. Age-related differences in the functional connectivity of the hippocampus during memory encoding. Hippocampus. 13:572-586.
29. Grossman M, Cooke A, DeVita C, Alsop D, Detre J, Chen W, Gee J. 2002. Age-related changes in working memory during sentence comprehension: an fMRI study. Neuroimage. 15:302-317.
30. Gutchess AH, Welsh RC, Hedden T, Bangeert A, Minear M, Liu LL, Park DC. 2005. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medialtemporal activity. J Cogn Neurosci. 17:84-96.
31. Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW. 1999. "Sparse" temporal sampling in auditory fMRI. Hum Brain Mapp. 7:213-223.
32. Hickok G, Poeppel D. 2007. The cortical organization of speech processing. Nat Rev Neurosci. 8:393-402.
33. Humphries C, Binder JR, Medler DA, Liebenthal E. 2006. Syntactic and semantic modulation of neural activity during auditory sentence comprehension. J Cogn Neurosci. 18:665-679.
34. Jonides J, Schumacher EH, Smith EE, Koeppe RA, Awh E, Reuter-Lorenz PA, Marshuetz C, Willis CR. 1998. The role of parietal cortex in verbal working memory. J Neurosci. 18:5026-5034.
35. Jonides J, Schumacher EH, Smith EE, Lauber EJ, Awh E, Minoshima S, Koeppe RA. 1997. Verbal working memory load affects regional brain activation as measured by PET. J Cogn Neurosci. 9:462-475.
36. Just MA, Carpenter PA. 1992. A capacity theory of comprehension: individual differences in working memory. Psychol Rev. 99:122-149.
37. Just MA, Carpenter PA, Keller TA, Eddy WF, Thulborn KR. 1996. Brain activation modulated by sentence comprehension. Science. 274:114-116.
38. Kaan E, Swaab TY. 2002. The brain circuitry of syntactic comprehension. Trends Cogn Sci. 6:350-356.
39. Keller TA, Carpenter PA, Just MA. 2001. The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. Cereb Cortex. 11:223-237.
40. Kemper S. 1986. Imitation of complex syntactic constructions by elderly adults. Appl Psycholinguist. 7:277-287.
41. Kemper S. 1987. Life span changes in syntactic complexity. J Gerontol. 42:323-328.
42. Kemper S, Marquis J, Thompson M. 2001. Longitudinal change in language production: effects of aging and dementia on grammatical complexity and propositional content. Psychol Aging. 16: 600-614.
43. Kotz SA, Cappa SF, von Cramon DY, Friederici A. 2002. Modulation of the lexical-semantic network by auditory semantic priming: an event-related functional MRI study. Neuroimage. 17: 1761-1772.
44. Libon DJ, Xie SX, Moore P, Farmer J, Antani S, McCawley G, Cross K, Grossman M. 2007. Patterns of neuropsychological impairment in frontotemporal dementia. Neurology. 68:369-375.
45. Liddle PF, Kiehl KA, Smith AM. 2001. Event-related fMRI study of response inhibition. Hum Brain Mapp. 12:100-109.
46. Madden DJ, Spaniol J, Costello MC, Bucur B, White LE, Cabeza R, Davis SW, Dennis NA, Provenzale JM, Huettel SA. 2009. Cerebral white matter integrity mediates adult age differences in cognitive performance. J Cogn Neurosci. 21:289-302.
47. Moulines E, Charpentier F. 1990. Pitch-synchronous waveform processing techniques for text-to-speech synthesis using diphones. Speech Commun. 9:453-467.
48. Ni W, Constable RT, Mencl WE, Pugh KR, Fulbright RK, Shaywitz SE, Shaywitz BA, Gore JC, Shankweiler D. 2000. An event-related neuroimaging study distinguishing form and content in sentence processing. J Cogn Neurosci. 12:120-133.
49. Obler LK, Fein D, Nicholas M, Albert ML. 1991. Auditory comprehension and aging: decline in syntactic processing. Appl Psycholinguist. 12:433-452.
50. Orfanidou E, Marslen-Wilson WD, Davis MH. 2006. Neural response suppression predicts repetition priming of spoken words and pseudowords. J Cogn Neurosci. 18:1237-1252.
51. Park DC, Polk TA, Park R, Minear M, Savage A, Smith MR. 2004. Aging reduces neural specialization in ventral visual cortex. Proc Natl Acad Sci USA. 101:13091-13095.
52. Peelle JE, Cooke A, Moore P, Vesely L, Grossman M. 2007. Syntactic and thematic components of sentence processing in progressive non-fluent aphasia and nonaphasic frontotemporal dementia. J Neurolinguistics. 20:482-494.
53. Peelle JE, Grossman M. 2008. Language processing in frontotemporal dementia: a brief review. Lang Linguistics Compass. 2:18-35.
54. Peelle JE, McMillan C, Moore P, Grossman M, Wingfield A. 2004. Dissociable patterns of brain activity during comprehension of rapid and syntactically complex speech: evidence from fMRI. Brain Lang. 91:315-325.
55. Peelle JE, Troiani V, Grossman M. 2009. Interaction between process and content in semantic memory: an fMRI study of noun feature knowledge. Neuropsychologia. 47:995-1003.
56. Peelle JE, Troiani V, Gee J, Moore P, McMillan C, Vesely L, Grossman M. 2008. Sentence comprehension and voxel-based morphometry in progressive nonfluent aphasia, semantic dementia, and nonaphasic frontotemporal dementia. J Neurolinguistics. 21:418-432.
57. Peelle JE, Wingfield A. 2005. Dissociations in perceptual learning revealed by adult age differences in adaptation to time-compressed speech. J Exp Psychol Hum Percept Perform. 31:1315-1330.
58. Prinz AA, Bucher D, Marder E. 2004. Similar network activity from disparate circuit parameters. Nat Neurosci. 7:1345-1352.
59. Raettig T, Kotz SA. 2008. Auditory processing of different types of pseudo-words: an event-related fMRI study. Neuroimage. 39: 1420-1428.
60. Rahman S, Sahakian BJ, Hodges JR, Rogers RD, Robbins TW. 1999. Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain. 122:1469-1493.
61. Reilly J, Troiani V, Grossman M, Wingfield A. 2007. An introduction to hearing loss and screening procedures for behavioral research. Behav Res Methods. 39:667-672.
62. Rodd JM, Davis MH, Johnsrude IS. 2005. The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. Cereb Cortex. 15:1261-1269.
63. Rypma B, Prabhakaran V, Desmond JE, Glover GH, Gabrieli JD. 1999. Load-dependent roles of frontal brain regions in the maintenance of working memory. Neuroimage. 9:216-226.
64. Salat DH, Buckner RL, Snyder AZ, Greve DN, Desikan RSR, Busa E, Morris JC, Dale AM, Fischl B. 2004. Thinning of the cerebral cortex in aging. Cereb Cortex. 14:721-730.
65. Swick D, Ashley V, Turken AU. 2008. Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci. 9:102.
66. Taylor PC, Nobre AC, Rushworth MFS. 2007. Subsecond changes in top-down control exerted by human medial frontal cortex during conflict and action selection: a combined transcranial magnetic stimulation-electroencephalography study. J Neurosci. 27: 11343-11353.
67. Thompson-Schill SL, D'Esposito M, Aguirre GK, Farah MJ. 1997. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc Natl Acad Sci USA. 94:14792-14797.
68. Troiani V, Fernández-Seara MA, Wang Z, Detre JA, Ash S, Grossman M. 2008. Narrative speech production: an fMRI study using continuous arterial spin labeling. Neuroimage. 40:932-939.
69. Vandenberghe R, Nobre AC, Price CJ. 2002. The response of left temporal cortex to sentences. J Cogn Neurosci. 14:550-560.
70. Vos SH, Gunter TC, Schriefers H, Friederici AD. 2001. Syntactic parsing and working memory: the effects of syntactic complexity, reading span, and concurrent load. Lang Cogn Process. 16:65-103.
71. Waters GS, Caplan D. 2004. Verbal working memory and on-line syntactic processing: evidence from self-paced listening. Q J Exp Psychol. 57A:129-163.
72. Wingfield A, Stine-Morrow EAL. 2000. Language and speech. In: Craik FIM, Salthouse TA, editors. The handbook of aging and cognition. 2nd ed. Mahwah (NJ): Lawrence Erlbaum Associates. p. 359-416.
73. Wingfield A, Grossman M. 2006. Language and the aging brain: patterns of neural compensation revealed by functional brain imaging. J Neurophysiol. 96:2830-2839.
74. Wingfield A, Peelle JE, Grossman M. 2003. Speech rate and syntactic complexity as multiplicative factors in speech comprehension by young and older adults. Aging Neuropsychol Cogn. 10: 310-322.
75. Worsley KJ, Evans AC, Marrett S, Neelin P. 1992. A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab. 12:900-918.
76. Xue G, Aron AR, Poldrack RA. 2008. Common neural substrates for1 inhibition of spoken and manual responses. Cereb Cortex. 18:1923-1932.
77. Zachary R. 1986. Shipley Institute for Living Scale. Los Angeles: Western Psychological Services.