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Neuropsychologia
06 06, 2023;184 108530.

The eyes speak when the mouth cannot: Using eye movements to interpret omissions in primary progressive aphasia.

M J Nelson, S Moeller, M Seckin, E J Rogalski, M-M Mesulam, R S Hurley
Author Information
  1. M J Nelson: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Neurological Surgery, Feinberg School of Medicine, Northwestern University, USA; Department of Neurosurgery, School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35249, USA. Electronic address: matthewnelson@uabmc.edu.
  2. S Moeller: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Psychology, University of Nevada, Las Vegas, NV 89154, USA.
  3. M Seckin: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Neurology, Acıbadem Mehmet Ali Aydınlar University School of Medicine, İstanbul, 34684, Turkey.
  4. E J Rogalski: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, USA.
  5. M-M Mesulam: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Neurology, Feinberg School of Medicine, Northwestern University, USA.
  6. R S Hurley: Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Feinberg School of Medicine, Northwestern University, Chicago, IL USA, 60611; Department of Psychology, Cleveland State University, Cleveland, OH, 44115, USA. Electronic address: r.s.hurley@csuohio.edu.
PMID: 36906222 DOI: 10.1016/j.neuropsychologia.2023.108530

Abstract

Though it may seem simple, object naming is a complex multistage process that can be impaired by lesions at various sites of the language network. Individuals with neurodegenerative disorders of language, known as primary progressive aphasias (PPA), have difficulty with naming objects, and instead frequently say "I don't know" or fail to give a vocal response at all, known as an omission. Whereas other types of naming errors (paraphasias) give clues as to which aspects of the language network have been compromised, the mechanisms underlying omissions remain largely unknown. In this study, we used a novel eye tracking approach to probe the cognitive mechanisms of omissions in the logopenic and semantic variants of PPA (PPA-L and PPA-S). For each participant, we identified pictures of common objects (e.g., animals, tools) that they could name aloud correctly, as well as pictures that elicited an omission. In a separate word-to-picture matching task, those pictures appeared as targets embedded among an array with 15 foils. Participants were given a verbal cue and tasked with pointing to the target, while eye movements were monitored. On trials with correctly-named targets, controls and both PPA groups ceased visual search soon after foveating the target. On omission trials, however, the PPA-S group failed to stop searching, and went on to view many foils "post-target". As further indication of impaired word knowledge, gaze of the PPA-S group was subject to excessive "taxonomic capture", such that they spent less time viewing the target and more time viewing related foils on omission trials. In contrast, viewing behavior of the PPA-L group was similar to controls on both correctly-named and omission trials. These results indicate that the mechanisms of omission in PPA differ by variant. In PPA-S, anterior temporal lobe degeneration causes taxonomic blurring, such that words from the same category can no longer be reliably distinguished. In PPA-L, word knowledge remains relatively intact, and omissions instead appear to be caused by downstream factors (e.g., lexical access, phonological encoding). These findings demonstrate that when words fail, eye movements can be particularly informative.

Keywords

anomia eye tracking object naming paraphasias primary progressive aphasia word comprehension

References

Psychol Rev. 1997 Oct;104(4):801-38 [PMID: 9337631]
Neurocase. 2016;22(1):65-75 [PMID: 25982291]
Brain. 2006 Aug;129(Pt 8):2132-47 [PMID: 16815878]
Acta Psychol (Amst). 2011 Jun;137(2):252-9 [PMID: 20864070]
Brain. 2013 Feb;136(Pt 2):601-18 [PMID: 23361063]
Neurology. 2011 May 24;76(21):1804-10 [PMID: 21606451]
Neuropsychologia. 2015 Sep;76:240-53 [PMID: 25585251]
J Exp Psychol Hum Learn. 1980 Mar;6(2):174-215 [PMID: 7373248]
Neuropsychologia. 2018 Aug;117:92-101 [PMID: 29802865]
Neurology. 2011 Mar 15;76(11):1006-14 [PMID: 21325651]
Annu Rev Psychol. 2012;63:1-29 [PMID: 21961947]
J Neuropsychol. 2019 Jun;13(2):183-197 [PMID: 29411521]
Nat Rev Neurol. 2014 Oct;10(10):554-69 [PMID: 25179257]
Arch Neurol. 2009 Dec;66(12):1545-51 [PMID: 20008661]
Brain. 2012 May;135(Pt 5):1537-53 [PMID: 22525158]
Cereb Cortex. 2020 Apr 14;30(4):2529-2541 [PMID: 31800048]
Brain Lang. 2008 Jan;104(1):24-32 [PMID: 17408733]
Neuropsychologia. 2007 Mar 14;45(5):1065-79 [PMID: 17074373]
Eur J Neurosci. 2001 Sep;14(5):869-76 [PMID: 11576191]
J Exp Psychol Hum Learn. 1980 Jul;6(4):391-9 [PMID: 7391754]
Neuropsychologia. 2008 Aug;46(10):2503-14 [PMID: 18499196]
J Neurolinguistics. 2016 Feb 1;37:68-81 [PMID: 26500393]
J Neurosci. 2012 Apr 4;32(14):4848-55 [PMID: 22492040]
Cogn Behav Neurol. 2019 Mar;32(1):46-53 [PMID: 30896577]
Ann Neurol. 2001 Apr;49(4):425-32 [PMID: 11310619]
Neuropsychology. 2019 Jan;33(1):13-34 [PMID: 30284872]
Perception. 2004;33(2):217-36 [PMID: 15109163]
Neuroimage. 2010 Jan 1;49(1):984-93 [PMID: 19679189]
Cogn Neuropsychol. 2013;30(3):172-93 [PMID: 24070176]
Neurology. 2008 Oct 14;71(16):1227-34 [PMID: 18633132]
Neurobiol Aging. 2020 Apr;88:71-82 [PMID: 31955981]
Brain. 2015 Aug;138(Pt 8):2423-37 [PMID: 26112340]
Cortex. 2018 Oct;107:188-203 [PMID: 28947063]
PLoS One. 2016 Feb 22;11(2):e0148707 [PMID: 26901052]
J Int Neuropsychol Soc. 2019 Nov;25(10):1011-1022 [PMID: 31511121]
J Alzheimers Dis. 2014;41(2):575-85 [PMID: 24662100]
Neuropsychol Rehabil. 2023 Mar;33(2):193-225 [PMID: 34775908]
J Neurosci. 2009 Dec 16;29(50):15762-9 [PMID: 20016092]
Cortex. 2016 Oct;83:39-50 [PMID: 27474916]
Cogn Neuropsychol. 2004 Mar 1;21(2):125-45 [PMID: 21038196]
Neuropsychology. 2010 Sep;24(5):581-9 [PMID: 20804246]
Brain Lang. 1985 Mar;24(2):266-83 [PMID: 3978406]
Brain. 1996 Apr;119 ( Pt 2):611-25 [PMID: 8800952]
Arch Neurol. 1969 Jan;20(1):82-9 [PMID: 4303441]

Grants

  1. R01 DC008552/NIDCD NIH HHS
  2. R01 AG077444/NIA NIH HHS
  3. T32 NS047987/NINDS NIH HHS
  4. P30 AG072977/NIA NIH HHS
  5. K01 DC019165/NIDCD NIH HHS
  6. P30 AG013854/NIA NIH HHS
  7. R01 AG056258/NIA NIH HHS
  8. UL1 TR001422/NCATS NIH HHS
  9. R01 NS075075/NINDS NIH HHS

MeSH Term

Humans
Eye Movements
Aphasia, Primary Progressive
Language
Semantics
Mouth
Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

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