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Neural correlates of auditory verbal short-term memory deficits in vascular and neurodegenerative aphasia

Nina F. Dronkers1, 2*, Stephen M. Wilson3, Juliana V. Baldo4, Bruce Miller5 and Maria Luisa Gorno-Tempini5
  • 1 University of California, Davis, United States
  • 2 University of California, Berkeley, United States
  • 3 Vanderbilt University Medical Center, United States
  • 4 Veterans Affairs Northern California Health Care System (VANCHCS), United States
  • 5 University of California, San Francisco, United States

Repetition deficits in brain-injured individuals may reflect disruptions of auditory verbal short-term memory (AVSTM) (Shallice & Warrington, 1977). Disruptions of AVSTM are apparent when patients lose the phonological trace of what they have just heard, yet retain the understanding of the sentence content. An example of this is hearing a low-frequency sentence such as “The pastry cook was elated” and responding “I don’t know, but it’s something about a happy baker” (Baldo et al, 2008). Though repetition deficits were classically associated with damage to the arcuate fasciculus, recent findings with lesion symptom mapping as well as functional imaging suggest posterior superior temporal or inferior parietal regions may be involved (e.g., Paulesu et al, 1993; Buchsbaum et al, 2011). The purpose of this study was to investigate the neural correlates of ASTVM by measuring the repetition of high- and low-frequency sentences in two groups of aphasic patients with different etiologies (vascular and neurodegenerative) using similar voxel-based anatomical analyses. Methods. 115 individuals who suffered a single left hemisphere infarction with persisting aphasia were included in the study. All were native English-speaking and right-handed with no prior neurologic or psychiatric history, and had brain imaging available for lesion reconstruction. In addition, 66 individuals with primary progressive aphasia (PPA) and neuroimaging data were recruited. To assess the AVSTM deficit, all patients’ scores on the Repetition subtest of the Western Aphasia Battery were divided into high- and low-frequency sentences, (e.g., “The telephone is ringing” vs “The pastry cook was elated”). The dependent measure was the difference in accuracy between these two sets of sentences. T1-weighted, high-resolution MRI scans were also obtained for each participant. Vascular patients’ lesions were computer-reconstructed and entered into a Voxel-based Lesion Symptom Mapping (VLSM) analysis (Bates et al, 2003) along with their repetition difference scores to identify brain regions associated with poor AVSTM. Voxel-Based Morphometry (VBM) was used to identify brain regions that correlated with poor AVSTM performance in the progressive patients. Both analyses were corrected for multiple comparisons using a permutation procedure (Wilson et al., 2010). Results. For the vascular patients, there was just one cluster where lesions were significantly associated with the repetition measure. This was located in the left posterior STG and angular gyrus (extent = 7880 mm3; p = 0.040) (Figure 1). For the PPA patients, there was also only one region where grey matter volume was correlated with the repetition measure. This cluster was also centered in the left posterior STG, and also extended into the angular gyrus (extent = 6992 mm3; p = 0.017) (Figure 1). Conclusions: Using anatomical-behavioral analyses, the same focal anatomical correlates of low-frequency sentence repetition were demonstrated in aphasic individuals with two very different etiologies. The posterior superior temporal gyrus was revealed as a critical area for the repetition of low- but not high-frequency sentences, suggesting an important role for this region in auditory short-term verbal memory mechanisms.

Figure 1
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Acknowledgements

This work was supported by the National Institutes of Health [NIDCD RO1 DC016345, NINDS R01 NS050915, NIA P50 AG03006, NIA P01 AG019724] and the U.S. Department of Veterans Affairs Office of Research & Development CSR&D Program.

References

Baldo, J. V., Klostermann, E. C., & Dronkers, N. F. (2008). It's either a cook or a baker: patients with conduction aphasia get the gist but lose the trace. Brain and Language, 105(2), 134-140. Bates, E., Wilson, S. M., Saygin, A. P., Dick, F., Sereno, M. I., Knight, R. T., & Dronkers, N. F. (2003). Voxel-based lesion-symptom mapping. Nature Neuroscience, 6, 448–450. Buchsbaum, B. R., Baldo, J., Okada, K., Berman, K. F., Dronkers, N. F., D'Esposito, M., et al. (2011). Conduction aphasia, sensory-motor integration, and phonological short-term memory – an aggregate analysis of lesion and fMRI data. Brain Lang. 119, 119–128. Paulesu, E., Frith, C. D., & Frackowiak, R. S. (1993). The neural correlates of the verbal component of working memory. Nature, 362(6418), 342-345. Shallice, T., & Warrington, E. K. (1977). Auditory-verbal short-term memory impairment and conduction aphasia. Brain and Language, 4(4), 479-491. Wilson, S. M., Henry, M. L., Besbris, M., Ogar, J. M., Dronkers, N. F., Jarrold, W., … Gorno-Tempini, M. L. (2010). Connected speech production in three variants of primary progressive aphasia. Brain, 133(7), 2069–2088.

Keywords: Aphasia after stroke, PPA, VLSM = voxel-based lesion-symptom mapping, VBM = voxel-based morphometry, Auditory verbal memory

Conference: Academy of Aphasia 57th Annual Meeting, Macau, Macao, SAR China, 27 Oct - 29 Oct, 2019.

Presentation Type: Platform presentation

Topic: Not eligible for student award

Citation: Dronkers NF, Wilson SM, Baldo JV, Miller B and Gorno-Tempini M (2019). Neural correlates of auditory verbal short-term memory deficits in vascular and neurodegenerative aphasia. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00107

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Received: 07 May 2019; Published Online: 09 Oct 2019.

* Correspondence: Mx. Nina F Dronkers, University of California, Davis, Davis, United States, dronkers@berkeley.edu