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Recovery of word form processing after left inferior parietal lesion: A single case fMRI study
Brain and Language 87 (2003) 124–125 www.elsevier.com/locate/b&l
Recovery of word form processing after left inferior parietal lesion: A single case fMRI study Marion Grande,* Susanne Weis, Klaus Willmes, and Walter Huber Aachen University of Technology (RWTH), 52062 Aachen, Germany
Introduction Several neuroimaging studies have demonstrated specific neural correlates of word processing in normal subjects as well as functional reorganisation after brain damage. Alternative hypotheses for mechanisms underlying reorganisation are still under debate. While some studies found predominantly right-hemisphere activation (e.g., Weiller et al., 1995), others reported (re)activation of left-hemisphere regions including perilesional areas (e.g., Zahn et al., 2002). These activations can represent functional take-over either in spared parts of a preexisting language system (‘redundancy recovery’) or in areas which are not related to the language system (‘vicarious functioning’) (cf., Marshall, 1984). In a previous fMRI study we demonstrated different cortical networks for the processing of word forms and concepts in normal subjects (Weis, Grande, Pollrich, Willmes, & Huber, 2001). The word form task required finding a homonym, which lead to bilateral activation of the inferior parietal cortex (BA 39, 40). In contrast, the conceptual association task yielded activation of Broca’s area and adjacent prefrontal cortex indicating lexical–semantic search. Using the same paradigm, we studied the patient RM who suffered from a left hemisphere lesion affecting the critical inferior parietal area. Our aim was to further investigate the mechanisms of functional recovery of lexical and semantic abilities. Given the fact that RM was able to solve both tasks sufficiently, we expected normal activation for the conceptual association task and redundancy effects for the homonym task as this task was particularly affected by the lesion.
meaning related to one of the two stimuli (e.g., river – money fi bank). (2) Finding a similarity, i.e., a conceptual associate, between two stimuli (e.g., river – lake fi water, boat, etc.). Functional image acquisition and analysis were identical to the normal group study.
Results RM solved 15 of the 42 homonym items correctly (normal subjects: mean 20.5; range 12–29). As expected RM showed a similar pattern of activation as the normal subjects. However there were a few striking differences, which mainly affected the homonym task (cf. Fig. 1).
Homonyms •
•
Method • Five months post onset we examined RM, a 32-year-old, male patient with residual aphasic symptoms. His left-hemisphere lesion resulting from MCA infarction involved the angular gyrus and the adjacent part of the supramarginal gyrus as well as the posterior insula and the posterior superior part of the middle temporal gyrus. He performed the following tasks (reported in Weis et al., 2001) on two visually presented German nouns: (1) Finding a homonym with each
*
Corresponding author. E-mail address: [email protected].
Solved items: Normal group data: activation of bilateral inferior parietal lobule (BA 39/40), precuneus (BA 7), and prefrontal areas (BA 9, 10). RM data: same as normals, additional activation of right inferior frontal (BA 44/45), left temporal (BA 20, 22), and perirolandic (BA 3, 4, 6) regions. Perirolandic activation was, in contrast to inferior frontal and temporal activations, not found in any normal subject. Unsolved items: Normal group data: bilateral occipital (BA 18/19) and left inferior frontal (BA 44/45) activations. RM data: same as normals, additional activation in bilateral temporal (BA 20, 21, 22, 42), bilateral but more left prefrontal (BA 6, 8, 9, 47), and superior parietal (BA 7) regions. All of these activations were observed in at least one of the normal subjects as well. Conceptual association: Normal group data: activations in bilateral occipital (BA 18/19), left frontal (BA 44/45, 47), and superior parietal (BA 7) regions. RM data: same as normals, except for absence of activation of Broca’s area (BA 44/45).
Discussion Overall RM showed the same activation pattern as the normal group: Unsolved homonyms as well as finding conceptual associates activated bilateral occipital and left frontal areas, which apparently
0093-934X/$ - see front matter 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0093-934X(03)00230-X
Abstract / Brain and Language 87 (2003) 124–125
125
Fig. 1. Significant activation in normal subjects (n = 15) and patient RM (hatched area = lesion) for solved items of the homonym task, projected onto standardized brain (SPM99; p < :001uncorr ; k = 15).
subserve semantic search. For solved homonyms mainly bilateral inferior parietal regions were found activated, which we consider to be crucial for word form knowledge. In addition to patterns of normal group activation, RM showed several additional activations which could indicate vicarious functioning. However, these additional activations were also found for at least one subject in the single case analysis. An exception is the left perirolandic activation underlying RM’s successful search for a homonym. This was not found in any of the 15 normal subjects and can therefore be interpreted as unrelated to word form knowledge as required by the homonym task. Since finding a homonym was the most demanding condition, this might reflect word form monitoring by means of inner speech as previously reported for silent recitation (Wildgruber, Ackermann, Klose, Kardatzki, & Grodd, 1996).
Conclusion We present a single case with damage to the word form system in the left hemisphere. In sum, the case of RM revealed mostly activations in areas activated by normal subjects as well and only few additional vicarious activation foci. With respect to the semantic network this finding had to be expected as the neural substrates were not damaged in RM. With respect to word form processing however the normal pattern of activation was achieved despite damage due to
perilesional activation of residual substrates. This finding is clearly in accordance with the assumption of redundancy recovery. In addition, vicarious functioning of speech motor cortex co-occurred. Most likely this reflects a compensatory strategy to activate specific word forms such as homonyms which was affected by the lesion.
References Marshall, J. F. (1984). Brain function: Neural adaptations and recovery from injury. Annual Review of Psychology, 35, 277–308. Weiller, C., Isensee, C., Rijntjes, M., & Huber, W, et al. (1995). Recovery from Wernicke’s aphasia: A positron emission tomographic study. Annals of Neurology, 37, 723–732. Weis, S., Grande, M., Pollrich, S., Willmes, K., & Huber, W. (2001). Processing of homonyms: A functional MRI study on the separation of word forms from concepts. Cortex, 37(5), 745–749. Wildgruber, D., Ackermann, H., Klose, U., Kardatzki, B., & Grodd, W. (1996). Functional lateralization of speech production at primary motor cortex: A fMRI study. Neuroreport, 7, 2791–2795. Zahn, R., Huber, W., Drews, E., Specht, K., Kemeny, S., Reith, W., Willmes, K., & Schwarz, M. (2002). Recovery of semantic word processing in transcortical sensory aphasia: A functional magnetic resonance imaging study. Neurocase, 8, 376–386.
Recovery of word form processing after left inferior parietal lesion: A single case fMRI study Marion Grande,* Susanne Weis, Klaus Willmes, and Walter Huber Aachen University of Technology (RWTH), 52062 Aachen, Germany
Introduction Several neuroimaging studies have demonstrated specific neural correlates of word processing in normal subjects as well as functional reorganisation after brain damage. Alternative hypotheses for mechanisms underlying reorganisation are still under debate. While some studies found predominantly right-hemisphere activation (e.g., Weiller et al., 1995), others reported (re)activation of left-hemisphere regions including perilesional areas (e.g., Zahn et al., 2002). These activations can represent functional take-over either in spared parts of a preexisting language system (‘redundancy recovery’) or in areas which are not related to the language system (‘vicarious functioning’) (cf., Marshall, 1984). In a previous fMRI study we demonstrated different cortical networks for the processing of word forms and concepts in normal subjects (Weis, Grande, Pollrich, Willmes, & Huber, 2001). The word form task required finding a homonym, which lead to bilateral activation of the inferior parietal cortex (BA 39, 40). In contrast, the conceptual association task yielded activation of Broca’s area and adjacent prefrontal cortex indicating lexical–semantic search. Using the same paradigm, we studied the patient RM who suffered from a left hemisphere lesion affecting the critical inferior parietal area. Our aim was to further investigate the mechanisms of functional recovery of lexical and semantic abilities. Given the fact that RM was able to solve both tasks sufficiently, we expected normal activation for the conceptual association task and redundancy effects for the homonym task as this task was particularly affected by the lesion.
meaning related to one of the two stimuli (e.g., river – money fi bank). (2) Finding a similarity, i.e., a conceptual associate, between two stimuli (e.g., river – lake fi water, boat, etc.). Functional image acquisition and analysis were identical to the normal group study.
Results RM solved 15 of the 42 homonym items correctly (normal subjects: mean 20.5; range 12–29). As expected RM showed a similar pattern of activation as the normal subjects. However there were a few striking differences, which mainly affected the homonym task (cf. Fig. 1).
Homonyms •
•
Method • Five months post onset we examined RM, a 32-year-old, male patient with residual aphasic symptoms. His left-hemisphere lesion resulting from MCA infarction involved the angular gyrus and the adjacent part of the supramarginal gyrus as well as the posterior insula and the posterior superior part of the middle temporal gyrus. He performed the following tasks (reported in Weis et al., 2001) on two visually presented German nouns: (1) Finding a homonym with each
*
Corresponding author. E-mail address: [email protected].
Solved items: Normal group data: activation of bilateral inferior parietal lobule (BA 39/40), precuneus (BA 7), and prefrontal areas (BA 9, 10). RM data: same as normals, additional activation of right inferior frontal (BA 44/45), left temporal (BA 20, 22), and perirolandic (BA 3, 4, 6) regions. Perirolandic activation was, in contrast to inferior frontal and temporal activations, not found in any normal subject. Unsolved items: Normal group data: bilateral occipital (BA 18/19) and left inferior frontal (BA 44/45) activations. RM data: same as normals, additional activation in bilateral temporal (BA 20, 21, 22, 42), bilateral but more left prefrontal (BA 6, 8, 9, 47), and superior parietal (BA 7) regions. All of these activations were observed in at least one of the normal subjects as well. Conceptual association: Normal group data: activations in bilateral occipital (BA 18/19), left frontal (BA 44/45, 47), and superior parietal (BA 7) regions. RM data: same as normals, except for absence of activation of Broca’s area (BA 44/45).
Discussion Overall RM showed the same activation pattern as the normal group: Unsolved homonyms as well as finding conceptual associates activated bilateral occipital and left frontal areas, which apparently
0093-934X/$ - see front matter 2003 Elsevier Science (USA). All rights reserved. doi:10.1016/S0093-934X(03)00230-X
Abstract / Brain and Language 87 (2003) 124–125
125
Fig. 1. Significant activation in normal subjects (n = 15) and patient RM (hatched area = lesion) for solved items of the homonym task, projected onto standardized brain (SPM99; p < :001uncorr ; k = 15).
subserve semantic search. For solved homonyms mainly bilateral inferior parietal regions were found activated, which we consider to be crucial for word form knowledge. In addition to patterns of normal group activation, RM showed several additional activations which could indicate vicarious functioning. However, these additional activations were also found for at least one subject in the single case analysis. An exception is the left perirolandic activation underlying RM’s successful search for a homonym. This was not found in any of the 15 normal subjects and can therefore be interpreted as unrelated to word form knowledge as required by the homonym task. Since finding a homonym was the most demanding condition, this might reflect word form monitoring by means of inner speech as previously reported for silent recitation (Wildgruber, Ackermann, Klose, Kardatzki, & Grodd, 1996).
Conclusion We present a single case with damage to the word form system in the left hemisphere. In sum, the case of RM revealed mostly activations in areas activated by normal subjects as well and only few additional vicarious activation foci. With respect to the semantic network this finding had to be expected as the neural substrates were not damaged in RM. With respect to word form processing however the normal pattern of activation was achieved despite damage due to
perilesional activation of residual substrates. This finding is clearly in accordance with the assumption of redundancy recovery. In addition, vicarious functioning of speech motor cortex co-occurred. Most likely this reflects a compensatory strategy to activate specific word forms such as homonyms which was affected by the lesion.
References Marshall, J. F. (1984). Brain function: Neural adaptations and recovery from injury. Annual Review of Psychology, 35, 277–308. Weiller, C., Isensee, C., Rijntjes, M., & Huber, W, et al. (1995). Recovery from Wernicke’s aphasia: A positron emission tomographic study. Annals of Neurology, 37, 723–732. Weis, S., Grande, M., Pollrich, S., Willmes, K., & Huber, W. (2001). Processing of homonyms: A functional MRI study on the separation of word forms from concepts. Cortex, 37(5), 745–749. Wildgruber, D., Ackermann, H., Klose, U., Kardatzki, B., & Grodd, W. (1996). Functional lateralization of speech production at primary motor cortex: A fMRI study. Neuroreport, 7, 2791–2795. Zahn, R., Huber, W., Drews, E., Specht, K., Kemeny, S., Reith, W., Willmes, K., & Schwarz, M. (2002). Recovery of semantic word processing in transcortical sensory aphasia: A functional magnetic resonance imaging study. Neurocase, 8, 376–386.