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Action processing and mirror neuron function in patients with amyotrophic lateral sclerosis: an fMRI study.

Jelsone-Swain L, Persad C, Burkard D, Welsh RC - PLoS ONE (2015)

Bottom Line: These results support a compensatory response in the MNS during action processing.In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus.Implications for future research are discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of South Carolina Aiken, Aiken, SC, United States of America; Department of Radiology, University of Michigan, Ann Arbor, MI, United States of America.

ABSTRACT
Amyotrophic lateral sclerosis (ALS) is a highly debilitating and rapidly fatal neurodegenerative disease. It has been suggested that social cognition may be affected, such as impairment in theory of mind (ToM) ability. Despite these findings, research in this area is scarce and the investigation of neural mechanisms behind such impairment is absent. Nineteen patients with ALS and eighteen healthy controls participated in this study. Because the mirror neuron system (MNS) is thought to be involved in theory of mind, we first implemented a straightforward action-execution and observation task to assess basic MNS function. Second, we examined the social-cognitive ability to understand actions of others, which is a component of ToM. We used fMRI to assess BOLD activity differences between groups during both experiments. Theory of mind was also measured behaviorally using the Reading the Mind in the Eyes test (RME). ALS patients displayed greater BOLD activity during the action-execution and observation task, especially throughout right anterior cortical regions. These areas included the right inferior operculum, premotor and primary motor regions, and left inferior parietal lobe. A conjunction analysis showed significantly more co-activated voxels during both the observation and action-execution conditions in the patient group throughout MNS regions. These results support a compensatory response in the MNS during action processing. In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus. Lastly, action understanding performance was able to cluster patients with ALS into high and lower performing groups, which then differentiated RME performance. Collectively, these data suggest that social cognition, particularly theory of mind, may be affected in a subset of patients with ALS. This impairment may be related to functioning of the MNS and other regions related to action processing and understanding. Implications for future research are discussed.

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Experiment 1 Action Observation and Execution Task, ALS > HC.Greater activity in the ALS group compared to HCs throughout the frontal lobe during the action observation and execution conditions.)
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pone.0119862.g003: Experiment 1 Action Observation and Execution Task, ALS > HC.Greater activity in the ALS group compared to HCs throughout the frontal lobe during the action observation and execution conditions.)

Mentions: Nineteen patients with ALS and sixteen HCs were included in these results. Between-group analyses in Experiment 1 showed greater activity in the ALS group compared to HCs for all three contrast conditions. Greater activity was observed throughout the MNS, particularly in the right hemisphere. Notably, the right inferior operculum was more active in the ALS group for all three contrasts (observe, execute, observe + execute), p < 0.001 (uncorrected, see Figs 3 and 4). There was also greater activity in left inferior parietal lobe and left middle temporal gyrus during both the observe and observe + execute contrasts. The main condition of interest, the observe condition, resulted in increased activity throughout the right frontal lobe including the supplementary motor area and rolandic operculum, the right parietal and temporal lobes, and the basal ganglia and cerebellum. The observe + execute contrast also recruited greater right frontal, parietal, and superior temporal gyrus activity as well as increased activity in the left primary motor cortex, left subcortical regions, and cerebellum. In accordance with previous literature, the motor execution condition resulted in greater activity in the ALS group compared to HCs. Specifically, activity was greater in the right premotor region (see Fig 3), right somatosensory cortex, right middle temporal gyrus, and left basal ganglia. The HC group exhibited no regions of greater activity compared to the ALS group in any contrast. See Table 3 for complete results.


Action processing and mirror neuron function in patients with amyotrophic lateral sclerosis: an fMRI study.

Jelsone-Swain L, Persad C, Burkard D, Welsh RC - PLoS ONE (2015)

Experiment 1 Action Observation and Execution Task, ALS > HC.Greater activity in the ALS group compared to HCs throughout the frontal lobe during the action observation and execution conditions.)
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401664&req=5

pone.0119862.g003: Experiment 1 Action Observation and Execution Task, ALS > HC.Greater activity in the ALS group compared to HCs throughout the frontal lobe during the action observation and execution conditions.)
Mentions: Nineteen patients with ALS and sixteen HCs were included in these results. Between-group analyses in Experiment 1 showed greater activity in the ALS group compared to HCs for all three contrast conditions. Greater activity was observed throughout the MNS, particularly in the right hemisphere. Notably, the right inferior operculum was more active in the ALS group for all three contrasts (observe, execute, observe + execute), p < 0.001 (uncorrected, see Figs 3 and 4). There was also greater activity in left inferior parietal lobe and left middle temporal gyrus during both the observe and observe + execute contrasts. The main condition of interest, the observe condition, resulted in increased activity throughout the right frontal lobe including the supplementary motor area and rolandic operculum, the right parietal and temporal lobes, and the basal ganglia and cerebellum. The observe + execute contrast also recruited greater right frontal, parietal, and superior temporal gyrus activity as well as increased activity in the left primary motor cortex, left subcortical regions, and cerebellum. In accordance with previous literature, the motor execution condition resulted in greater activity in the ALS group compared to HCs. Specifically, activity was greater in the right premotor region (see Fig 3), right somatosensory cortex, right middle temporal gyrus, and left basal ganglia. The HC group exhibited no regions of greater activity compared to the ALS group in any contrast. See Table 3 for complete results.

Bottom Line: These results support a compensatory response in the MNS during action processing.In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus.Implications for future research are discussed.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of South Carolina Aiken, Aiken, SC, United States of America; Department of Radiology, University of Michigan, Ann Arbor, MI, United States of America.

ABSTRACT
Amyotrophic lateral sclerosis (ALS) is a highly debilitating and rapidly fatal neurodegenerative disease. It has been suggested that social cognition may be affected, such as impairment in theory of mind (ToM) ability. Despite these findings, research in this area is scarce and the investigation of neural mechanisms behind such impairment is absent. Nineteen patients with ALS and eighteen healthy controls participated in this study. Because the mirror neuron system (MNS) is thought to be involved in theory of mind, we first implemented a straightforward action-execution and observation task to assess basic MNS function. Second, we examined the social-cognitive ability to understand actions of others, which is a component of ToM. We used fMRI to assess BOLD activity differences between groups during both experiments. Theory of mind was also measured behaviorally using the Reading the Mind in the Eyes test (RME). ALS patients displayed greater BOLD activity during the action-execution and observation task, especially throughout right anterior cortical regions. These areas included the right inferior operculum, premotor and primary motor regions, and left inferior parietal lobe. A conjunction analysis showed significantly more co-activated voxels during both the observation and action-execution conditions in the patient group throughout MNS regions. These results support a compensatory response in the MNS during action processing. In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus. Lastly, action understanding performance was able to cluster patients with ALS into high and lower performing groups, which then differentiated RME performance. Collectively, these data suggest that social cognition, particularly theory of mind, may be affected in a subset of patients with ALS. This impairment may be related to functioning of the MNS and other regions related to action processing and understanding. Implications for future research are discussed.

Show MeSH
Related in: MedlinePlus