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Published in: Alzheimer's Research & Therapy 1/2017

Open Access 01-12-2017 | Research

Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias

Authors: Chris J. D. Hardy, Jennifer L. Agustus, Charles R. Marshall, Camilla N. Clark, Lucy L. Russell, Rebecca L. Bond, Emilie V. Brotherhood, David L. Thomas, Sebastian J. Crutch, Jonathan D. Rohrer, Jason D. Warren

Published in: Alzheimer's Research & Therapy | Issue 1/2017

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Abstract

Background

Non-verbal auditory impairment is increasingly recognised in the primary progressive aphasias (PPAs) but its relationship to speech processing and brain substrates has not been defined. Here we addressed these issues in patients representing the non-fluent variant (nfvPPA) and semantic variant (svPPA) syndromes of PPA.

Methods

We studied 19 patients with PPA in relation to 19 healthy older individuals. We manipulated three key auditory parameters—temporal regularity, phonemic spectral structure and prosodic predictability (an index of fundamental information content, or entropy)—in sequences of spoken syllables. The ability of participants to process these parameters was assessed using two-alternative, forced-choice tasks and neuroanatomical associations of task performance were assessed using voxel-based morphometry of patients’ brain magnetic resonance images.

Results

Relative to healthy controls, both the nfvPPA and svPPA groups had impaired processing of phonemic spectral structure and signal predictability while the nfvPPA group additionally had impaired processing of temporal regularity in speech signals. Task performance correlated with standard disease severity and neurolinguistic measures. Across the patient cohort, performance on the temporal regularity task was associated with grey matter in the left supplementary motor area and right caudate, performance on the phoneme processing task was associated with grey matter in the left supramarginal gyrus, and performance on the prosodic predictability task was associated with grey matter in the right putamen.

Conclusions

Our findings suggest that PPA syndromes may be underpinned by more generic deficits of auditory signal analysis, with a distributed cortico-subcortical neuraoanatomical substrate extending beyond the canonical language network. This has implications for syndrome classification and biomarker development.
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Literature
1.
go back to reference Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, et al. Classification of primary progressive aphasia and its variants. Neurology. 2011;76:1006–14.CrossRefPubMedPubMedCentral Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, et al. Classification of primary progressive aphasia and its variants. Neurology. 2011;76:1006–14.CrossRefPubMedPubMedCentral
2.
go back to reference Rogalski E, Cobia D, Harrison TM, Wieneke C, Weintraub S, Mesulam MM. Progression of language decline and cortical atrophy in subtypes of primary progressive aphasia. Neurology. 2011;76:1804–10.CrossRefPubMedPubMedCentral Rogalski E, Cobia D, Harrison TM, Wieneke C, Weintraub S, Mesulam MM. Progression of language decline and cortical atrophy in subtypes of primary progressive aphasia. Neurology. 2011;76:1804–10.CrossRefPubMedPubMedCentral
3.
4.
go back to reference Bozeat S, Lambon-Ralph MA, Patterson K, Garrard P, Hodges JR. Non-verbal semantic impairment in semantic dementia. Neuropsychologia. 2000;38:1207–15.CrossRefPubMed Bozeat S, Lambon-Ralph MA, Patterson K, Garrard P, Hodges JR. Non-verbal semantic impairment in semantic dementia. Neuropsychologia. 2000;38:1207–15.CrossRefPubMed
5.
go back to reference Goll JC, Crutch SJ, Loo JHY, Rohrer JD, Frost C, Bamiou D-E, et al. Non-verbal sound processing in the primary progressive aphasias. Brain. 2010;133:272–85.CrossRefPubMed Goll JC, Crutch SJ, Loo JHY, Rohrer JD, Frost C, Bamiou D-E, et al. Non-verbal sound processing in the primary progressive aphasias. Brain. 2010;133:272–85.CrossRefPubMed
6.
7.
go back to reference Hailstone JC, Ridgway GR, Bartlett JW, Goll JC, Buckley AH, Crutch SJ, et al. Voice processing in dementia: a neuropsychological and neuroanatomical analysis. Brain. 2011;134:2535–47.CrossRefPubMedPubMedCentral Hailstone JC, Ridgway GR, Bartlett JW, Goll JC, Buckley AH, Crutch SJ, et al. Voice processing in dementia: a neuropsychological and neuroanatomical analysis. Brain. 2011;134:2535–47.CrossRefPubMedPubMedCentral
10.
go back to reference Golden HL, Downey LE, Fletcher PD, Mahoney CJ, Schott JM, Mummery CJ, et al. Identification of environmental sounds and melodies in syndromes of anterior temporal lobe degeneration. J Neurol Sci. 2015;352:94–8.CrossRefPubMedPubMedCentral Golden HL, Downey LE, Fletcher PD, Mahoney CJ, Schott JM, Mummery CJ, et al. Identification of environmental sounds and melodies in syndromes of anterior temporal lobe degeneration. J Neurol Sci. 2015;352:94–8.CrossRefPubMedPubMedCentral
11.
go back to reference Golden HL, Clark CN, Nicholas JM, Cohen MH, Slattery CF, Paterson RW, et al. Music perception in dementia. J Alzheimers Dis. 2016;55:933–49.CrossRef Golden HL, Clark CN, Nicholas JM, Cohen MH, Slattery CF, Paterson RW, et al. Music perception in dementia. J Alzheimers Dis. 2016;55:933–49.CrossRef
12.
go back to reference Grube M, Bruffaerts R, Schaeverbeke J, Neyens V, De Weer A-S, Seghers A, et al. Core auditory processing deficits in primary progressive aphasia. Brain. 2016;139:1817–29.CrossRefPubMedPubMedCentral Grube M, Bruffaerts R, Schaeverbeke J, Neyens V, De Weer A-S, Seghers A, et al. Core auditory processing deficits in primary progressive aphasia. Brain. 2016;139:1817–29.CrossRefPubMedPubMedCentral
14.
go back to reference Rohrer JD, Lashley T, Schott JM, Warren JE, Mead S, Isaacs AM, et al. Clinical and neuroanatomical signatures of tissue pathology in frontotemporal lobar degeneration. Brain. 2011;134:2565–81.CrossRefPubMedPubMedCentral Rohrer JD, Lashley T, Schott JM, Warren JE, Mead S, Isaacs AM, et al. Clinical and neuroanatomical signatures of tissue pathology in frontotemporal lobar degeneration. Brain. 2011;134:2565–81.CrossRefPubMedPubMedCentral
15.
go back to reference Lambon Ralph MA, Sage K, Jones RW, Mayberry EJ. Coherent concepts are computed in the anterior temporal lobes. Proc Natl Acad Sci U S A. 2010;107:2717–22.CrossRefPubMedPubMedCentral Lambon Ralph MA, Sage K, Jones RW, Mayberry EJ. Coherent concepts are computed in the anterior temporal lobes. Proc Natl Acad Sci U S A. 2010;107:2717–22.CrossRefPubMedPubMedCentral
16.
go back to reference Lambon Ralph MA, Jefferies E, Patterson K, Rogers TT. The neural and computational bases of semantic cognition. Nat Rev Neurosci. 2017;18:42–55.CrossRef Lambon Ralph MA, Jefferies E, Patterson K, Rogers TT. The neural and computational bases of semantic cognition. Nat Rev Neurosci. 2017;18:42–55.CrossRef
18.
go back to reference Henry ML, Wilson SM, Babiak MC, Mandelli ML, Beeson PM, Miller ZA, et al. Phonological processing in primary progressive aphasia. J Cogn Neurosci. 2016;28:210–22.CrossRefPubMed Henry ML, Wilson SM, Babiak MC, Mandelli ML, Beeson PM, Miller ZA, et al. Phonological processing in primary progressive aphasia. J Cogn Neurosci. 2016;28:210–22.CrossRefPubMed
19.
go back to reference Hsieh S, Hornberger M, Piguet O, Hodges JR. Neural basis of music knowledge: evidence from the dementias. Brain. 2011;134:2523–34.CrossRefPubMed Hsieh S, Hornberger M, Piguet O, Hodges JR. Neural basis of music knowledge: evidence from the dementias. Brain. 2011;134:2523–34.CrossRefPubMed
20.
go back to reference Griffiths TD, Warren JD. The planum temporale as a computational hub. Trends Neurosci. 2002;25:348–53.CrossRefPubMed Griffiths TD, Warren JD. The planum temporale as a computational hub. Trends Neurosci. 2002;25:348–53.CrossRefPubMed
21.
go back to reference Overath T, Cusack R, Kumar S, von Kriegstein K, Warren JD, Grube M, et al. An information theoretic characterisation of auditory encoding. PLoS Biol. 2007;5:e288.CrossRefPubMedPubMedCentral Overath T, Cusack R, Kumar S, von Kriegstein K, Warren JD, Grube M, et al. An information theoretic characterisation of auditory encoding. PLoS Biol. 2007;5:e288.CrossRefPubMedPubMedCentral
23.
go back to reference Cope TE, Grube M, Singh B, Burn DJ, Griffiths TD. The basal ganglia in perceptual timing: timing performance in multiple system atrophy and Huntington’s disease. Neuropsychologia. 2014;52:73–81.CrossRefPubMedPubMedCentral Cope TE, Grube M, Singh B, Burn DJ, Griffiths TD. The basal ganglia in perceptual timing: timing performance in multiple system atrophy and Huntington’s disease. Neuropsychologia. 2014;52:73–81.CrossRefPubMedPubMedCentral
24.
go back to reference Schaeverbeke J, Bruffaerts R, Grube M, Neyens V, Bergmans B, Dries E. Deficits in rhythm processing in PPA are linked to SMA atrophy. J Neurochem. 2016;1:222–428. Schaeverbeke J, Bruffaerts R, Grube M, Neyens V, Bergmans B, Dries E. Deficits in rhythm processing in PPA are linked to SMA atrophy. J Neurochem. 2016;1:222–428.
25.
26.
go back to reference Scott SK, Blank CC, Rosen S, Wise RJS. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 2000;123:2400–6.CrossRefPubMed Scott SK, Blank CC, Rosen S, Wise RJS. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 2000;123:2400–6.CrossRefPubMed
27.
go back to reference Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8:393–402.CrossRefPubMed Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8:393–402.CrossRefPubMed
28.
go back to reference Rauschecker JP, Scott SK. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 2009;12:718–24.CrossRefPubMedPubMedCentral Rauschecker JP, Scott SK. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 2009;12:718–24.CrossRefPubMedPubMedCentral
29.
go back to reference Blesser B. Speech perception under conditions of spectral transformation. J Speech Lang Hear Res. 1972;15:5–41.CrossRef Blesser B. Speech perception under conditions of spectral transformation. J Speech Lang Hear Res. 1972;15:5–41.CrossRef
30.
go back to reference Ridgway G, Omar R, Ourselin S, Hill D, Warren J, Fox N. Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage. 2009;44:99–111.CrossRefPubMed Ridgway G, Omar R, Ourselin S, Hill D, Warren J, Fox N. Issues with threshold masking in voxel-based morphometry of atrophied brains. Neuroimage. 2009;44:99–111.CrossRefPubMed
31.
go back to reference Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.CrossRefPubMed Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.CrossRefPubMed
32.
33.
go back to reference Hertrich I, Dietrich S, Ackermann H. The role of the supplementary motor area for speech and language processing. Neurosci Biobehav Rev. 2016;68:602–10.CrossRefPubMed Hertrich I, Dietrich S, Ackermann H. The role of the supplementary motor area for speech and language processing. Neurosci Biobehav Rev. 2016;68:602–10.CrossRefPubMed
34.
go back to reference Maruta C, Makhmood S, Downey LE, Golden HL, Fletcher PD, Witoonpanich P, et al. Delayed auditory feedback simulates features of nonfluent primary progressive aphasia. J Neurol Sci. 2014;347:345–8.CrossRefPubMedPubMedCentral Maruta C, Makhmood S, Downey LE, Golden HL, Fletcher PD, Witoonpanich P, et al. Delayed auditory feedback simulates features of nonfluent primary progressive aphasia. J Neurol Sci. 2014;347:345–8.CrossRefPubMedPubMedCentral
35.
go back to reference Grahn JA, Rowe JB. Finding and feeling the musical beat: striatal dissociations between detection and prediction of regularity. Cereb Cortex. 2013;23:913–21.CrossRefPubMed Grahn JA, Rowe JB. Finding and feeling the musical beat: striatal dissociations between detection and prediction of regularity. Cereb Cortex. 2013;23:913–21.CrossRefPubMed
36.
go back to reference Looi JCL, Walterfang M, Velakoulis D, Macfarlane MD, Svensson LA, Wahlund LO. Frontotemporal dementia as a frontostriatal disorder: neostriatal morphology as a biomarker and structural basis for an endophenotype. Aust N Z J Psychiatry. 2012;46:422–34.CrossRefPubMed Looi JCL, Walterfang M, Velakoulis D, Macfarlane MD, Svensson LA, Wahlund LO. Frontotemporal dementia as a frontostriatal disorder: neostriatal morphology as a biomarker and structural basis for an endophenotype. Aust N Z J Psychiatry. 2012;46:422–34.CrossRefPubMed
37.
go back to reference Mandelli ML, Caverzasi E, Binney RJ, Henry ML, Lobach I, Block N, et al. Frontal white matter tracts sustaining speech production in primary progressive aphasia. J Neurosci. 2014;34:9754–67.CrossRefPubMedPubMedCentral Mandelli ML, Caverzasi E, Binney RJ, Henry ML, Lobach I, Block N, et al. Frontal white matter tracts sustaining speech production in primary progressive aphasia. J Neurosci. 2014;34:9754–67.CrossRefPubMedPubMedCentral
38.
go back to reference Ravizza SM, Delgado MR, Chein JM, Becker JT, Fiez JA. Functional dissociations within the inferior parietal cortex in verbal working memory. Neuroimage. 2004;22:562–73.CrossRefPubMed Ravizza SM, Delgado MR, Chein JM, Becker JT, Fiez JA. Functional dissociations within the inferior parietal cortex in verbal working memory. Neuroimage. 2004;22:562–73.CrossRefPubMed
39.
go back to reference Haruno M, Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol. 2006;95:948–59.CrossRefPubMed Haruno M, Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol. 2006;95:948–59.CrossRefPubMed
40.
go back to reference Geiser E, Notter M, Gabrieli JDE. A corticostriatal neural system enhances auditory perception through temporal context processing. J Neurosci. 2012;32:6177–82.CrossRefPubMed Geiser E, Notter M, Gabrieli JDE. A corticostriatal neural system enhances auditory perception through temporal context processing. J Neurosci. 2012;32:6177–82.CrossRefPubMed
41.
go back to reference Nastase SA, Iacovella V, Davis B, Hasson U. Connectivity in the human brain dissociates entropy and complexity of auditory inputs. Neuroimage. 2015;108:292–300.CrossRefPubMedPubMedCentral Nastase SA, Iacovella V, Davis B, Hasson U. Connectivity in the human brain dissociates entropy and complexity of auditory inputs. Neuroimage. 2015;108:292–300.CrossRefPubMedPubMedCentral
Metadata
Title
Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias
Authors
Chris J. D. Hardy
Jennifer L. Agustus
Charles R. Marshall
Camilla N. Clark
Lucy L. Russell
Rebecca L. Bond
Emilie V. Brotherhood
David L. Thomas
Sebastian J. Crutch
Jonathan D. Rohrer
Jason D. Warren
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2017
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-017-0278-2

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