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The authors present three patients with acquired extroversion who met criteria for FTD. Therefore, there was less residual capacity to upregulate the activation for the dual-task from the single tasks. Using the extracted beta values, we calculated the upregulation from single-tasks to dual-task as follows:. Mean upregulation was calculated by averaging the upregulation per ROI.
Outliers were detected according to the outlier labeling rule cf. Independent t-tests were used to compare the upregulation between age groups. P-values were corrected for multiple comparisons. Fig 2A shows the group data for the performance on the balance task during the balance-only task and balance plus calculation dual-task.
Balance performance was significantly worse during dual- vs. Fig 2B shows the data for the percent of correct calculation trials during single- and dual-tasking. Mean DTC was calculated by averaging the performance decline from single- to dual-tasking for the balance and calculation task.
Table 2 lists the local maxima of activated clusters during balance, calculation and dual-task conditions. Fig 3A shows activation patterns as compared to baseline. Deactivation patterns are described in more detail in the supplementary material. Deactivations were evident mainly in occipital areas left cuneus, bilateral calcarine sulci, and left lingual gyrus. Voxel size is 3x3x3 mm. A: Mean brain activation patterns during balance and calculation upper panel , and dual-tasking lower panel as compared with baseline. Significantly activated voxels during balance, calculation and dual-tasking, i.
Voxels shown in red in the upper panel are those revealed by conjunction analysis balance AND calculation and therefore represent areas not specific for a single-task. B: Age-related differences during balance, calculation, and dual-tasking. Voxels with higher activation in old compared with young adults are shown in green, whereas voxels with higher activation in young compared with old adults are shown in purple.
During calculation, a large fronto-parietal network was activated, including the left SMA, bilateral precentral gyri, bilateral inferior and left superior parietal lobules, left middle frontal gyrus, right superior frontal gyrus. Also bilateral insular cortices, temporal gyri, caudate nuclei and parts of the cerebellum were active. During calculation widespread areas became deactivated, including bilateral medial and superior frontal areas, bilateral angular gyri, left cingulate gyrus, left superior and bilateral middle occipital gyri, and temporal areas.
Dual-tasking evoked an activation pattern combining those of the calculation and balance task and a deactivation pattern similar to that during calculation. Table 3 and Fig 3B display the local maxima of clusters with significantly different activations between young and old adults. During balance and dual-tasking, there were no brain regions for which the young adults showed higher activation than the old adults. However, during calculation, more activation was observed in the left precentral gyrus and SMA for young than for old adults.
In all three conditions, there were clusters with significantly higher activation in old as compared with young adults. During balance, old adults showed higher activation in motor right precentral gyrus and left paracentral lobule and sensory regions bilateral precuneus and cuneus. During calculation, main clusters with age-related activation increases were found in the bilateral precentral gyri and the left medial frontal gyrus.
These areas were also more activated in old adults during dual-tasking. Additionally, bilateral lingual gyri, right inferior and middle occipital gyrus, left calcarine sulcus, and left precuneus were more activated in old than in young adults during dual-tasking. Bar plots of the BOLD responses in the clusters with an age-related increase in activation during dual-tasking can be found in the supplementary material.
Using a multiple regression model, there were no significant relationships between brain activation and behavioral performance single-task performance and DTC in the brain regions showing age-related changes in brain activation. Table 2 shows that most brain regions involved in dual-tasking are also involved in balance or calculation, suggesting little to no dual-task specific activation. Indeed, when contrasting the dual-task condition with the sum of the single-task conditions, there were no significant clusters in either age group.
A conjunction analysis revealed eight clusters that were activated during both single-tasks in both age groups, including the SMA, right insula, bilateral premotor areas, cerebellum, and parietal lobules Table 4. These clusters were subjected to a ROI-analysis. Cluster size is given for the peak voxel per cluster. P-values for the age young, old by condition balance, calculation, dual-task interactions are given, with and without Bonferonni correction.
There were no significant correlations. As expected, we found greater dual-task cost DTC , increased brain activation, and decreased upregulation in the insula in old compared with young adults.
However, measures of brain activation and behavior did not correlate. We found no dual-task specific activation in either group. Therefore, under the current experimental conditions, neither structural interference nor dual-task specific activation could explain the age-related increase in DTC.
We consider our dual-task paradigm, comprising calculation plus simulated balancing, challenging and different in nature compared with previous studies that used finger sequencing [ 29 ] or visuomanual drawing and simple mental arithmetic [ 24 ]. Indeed, under such less challenging conditions it can be difficult to produce behavioral DTC [ 24 ].
We found lower performance levels and higher DTC in old compared with young adults when considering both calculation and balancing performance, but there was no significant effect of age on DTC when the tasks were considered separately. This may be because of a cancellation effect due to some subjects performing poorly on one task while other subjects performing poorly on the other task. Indeed, when looking at the individual scores, low performers on one task were not necessarily low performers on the other task. This means that in order to see the age effect on dual-task performance, performance changes in both tasks should be taken into account.
Although the condition vs. Nevertheless, activity patterns for the balance and calculation tasks were comparable to those reported in the literature. Imaging studies have often used arithmetic tasks and, as in the present study, consistently observed an increase in activation as compared to baseline of the frontal-parietal network [ 49 ]—[ 51 ].
Previous studies investigating the neural correlates of balance have used fMRI during mental imagery [ 39 ], [ 42 ], action observation [ 42 ], or a plantar flexion force control task [ 40 ], or PET-scans during actual standing [ 41 ]. Commonly activated areas consistent with the present study were the premotor cortex, prefrontal cortex, inferior and middle frontal gyrus, SMA, cerebellum, basal ganglia, thalamus, visual cortex, insula, and inferior parietal areas. The brain activation pattern we observed during the simulated balance task was remarkably similar to the activation pattern during the imagery and action observation of balancing [ 42 ], suggesting that perhaps our participants imagined themselves being the balancing avatar.
The external validity of the simulated balance task was further supported by a significant correlation with center of pressure fluctuations during upright standing. Consistent with previous fMRI studies [ 43 ], [ 62 ]—[ 69 ], old adults exhibited greater brain activation than young adults in all tasks.
Regarding balance tasks, age correlated with the activation of several multisensory areas during imaginary standing compared with lying [ 43 ]. We found age-related activation increases in both motor precentral and paracentral gyri and sensory cuneus and precuneus areas during the balance condition, possibly because our balance simulation was a real motor task instead of an imaginary motor task. During the calculation condition, the greatest cluster with an age-related increase in activation was located in the medial frontal gyrus.
This area belongs to the prefrontal gyrus, in which age-related increases in activation during performance of cognitive tasks are well-known [ 62 ], [ 70 ]. The functional meaning of the increased brain activation with aging is still under debate [ 23 ]. One theory is that old adults use the additional activation to compensate for structural and functional decline, predicting a positive correlation between activation and behavioral performance. Alternatively, the dedifferentiation theory suggests that the more widespread activation pattern results from an age-related loss in the ability to selectively recruit brain areas.
Consistent positive correlations between higher prefrontal activity and cognitive performance [ 71 ]—[ 74 ], as well as higher brain activity in various motor, parietal, frontal and cerebellar areas and motor performance [ 65 ], [ 75 ], strongly support the compensation theory. However, less neural specificity in visual areas for different stimulus categories faces, houses, pseudowords, and chairs in old compared with young adults [ 76 ], and negative correlations between age-related activation increases in ipsilateral motor areas and motor performance [ 64 ], [ 66 ], [ 77 ], show that at least in certain areas dedifferentiation occurs.
As before [ 24 ], we found no correlation between activation in the areas over-activated by old adults and single-task performance, implying that the additional activation did not impair nor did it improve performance. This suggests an age-related spreading of brain activity beyond functional focus, favoring the dedifferentiation over the compensation theory. However, we must be cautious with such a conclusion because our analyses might have been underpowered. The literature is inconsistent regarding dual-task specific activation: whereas some studies did find evidence for dual-tasking requiring activation additional to the sum of the single-tasks [ 26 ]—[ 29 ], [ 78 ]—[ 80 ], others did not [ 17 ], [ 24 ], [ 30 ], [ 31 ].
Probably, the dual-task specific activation is dependent on the single-tasks, and there is no common executive control system that is active for all types of dual-tasking [ 21 ], [ 81 ]. In the current study, we did not find any dual-task specific activation in young or old adults. Therefore, it is unlikely that the age-related dual-task performance deficits were due to inadequate dual-task specific activation.
Although no additional activation was found during dual-tasking, we cannot exclude that the underlying processes, such as temporal dynamics, interactions between neuronal populations, or connectivity patterns, were different between single- and dual-tasking or between age groups.
Volume 6 Issue 6 (2010)
The assessment of such processes would require different neurophysiological measures, such as EEG or time-resolved fMRI. Regardless of the functional meaning, we hypothesized that the higher activation in old adults would cause structural interference and therefore greater DTC. However, we found no correlation between brain activation and DTC in the areas with age-related differences in activation.
There are at least three possible explanations for this lack of correlation. First, the increased activation in old adults did not cause increased structural interference because the areas with higher activation were involved in only one of the two tasks. Second, old adults could still increase their brain activation from single- to dual-task, despite increased activation during single-tasks. Third, DTC was not related to structural interference. To examine whether old adults exhibited greater structural interference, we performed a series of ROI analyses. Eight brain regions were selected because of their involvement in both tasks in both age groups.
All regions, except the cerebellum, were expected to be activated in both tasks based on literature. We found an age by condition interaction in the right insula and left superior parietal lobule. Only in the right insula, however, there was an age-related increase in structural interference, quantified as a reduced activation-upregulation from single- to dual-task.
However, the amount of upregulation was not correlated with DTC, suggesting that dual-task performance was not affected by the structural interference. It may be that the age-related increase in structural interference in the right insula was too small to cause DTC, or that insular activation was not essential for task performance. Although that would explain the lack of correlation between upregulation and DTC, the observed increase in DTC with aging remains unexplained. Therefore it seems that, at least under the current experimental conditions, age-related increases in DTC were not due to greater structural interference.
Dialogues in Clinical Neuroscience
As neither structural interference nor dual-task specific activation could explain the age-related deficit in dual-task performance, we must consider alternative theories that could not be tested with the current experimental setup. One theory explaining DTC is the cross-talk model [ 82 ]. Cross-talk occurs when the effects of processing one task interfere with processing the other, and is therefore dependent on the content-based overlap between tasks and stimulus-response modalities [ 83 ], [ 84 ].
For example, DTC increased when the non-target words in one visual search task belonged to the target category in the other visual search task [ 83 ]. We believe that cross-talk was not a critical element in our experiment, as the tasks used did not have any content-based overlap, or incompatible or shared stimulus-response modalities. Moreover, there is no reason to think that age would affect the amount of cross-talk. Another theory for DTC is that there is a central bottleneck that can perform certain processes only sequentially, resulting in serial queuing and time delays [ 85 ].
There is quite convincing evidence from behavioral and time-resolved fMRI studies that a central bottleneck is indeed present when two discrete choice reaction time tasks are performed with a short interstimulus interval [ 82 ], [ 86 ], [ 87 ]. It is possible that also during continuous tasks certain processes cannot be performed in parallel, requiring subjects to rapidly switch between tasks. As aging is associated with reduced processing speed, time delays may be more pronounced and interfere with smooth performance.
Although evidence is lacking for healthy old adults, in multiple sclerosis patients processing speed indeed correlated with DTC when performing a cognitive task during gait or standing [ 88 ], [ 89 ]. To determine whether a central bottleneck can account for the age-related decline in dual-task performance, future research should use high-temporal resolution measures, such as time-resolved fMRI. However, the number of participants in our study 32 old adults, 23 young adults is high compared with similar studies [ 5 ], [ 24 ], [ 90 ], [ 91 ].
Furthermore, the scatter plots in Fig 5 show no trend for the negative correlation that would be expected based on the structural interference hypothesis and even show a tendency towards a positive correlation. Another methodological aspect to consider is whether the selection of tasks was optimal to test our hypothesis. The fact that we, in contrary to a previous study [ 24 ], did find increased dual-task costs and decreased upregulation with aging shows that the tasks were challenging enough and did cause structural interference.
We therefore believe that the negative findings in the present study were not due to methodological limitations. Another factor that may have influenced our results is head movement in the scanner, which was similar between conditions F 1. Therefore, it must remain speculative whether missing DT-specific activation in old adults might also be due to increased noise in the data caused by head movements.
In future studies, better control of head movements is thus required. However, we do believe that this had only a minor effect on our results, as we controlled for head movement by realigning the scans and using the obtained motion parameters as covariates in the fMRI analysis. In addition, we excluded subjects with excessive or task-related head movement.
Lastly, age-related changes in neurovascular coupling and morphology could have affected some of our results. As such changes should affect all conditions equally [ 92 ], it is highly unlikely that our main interest, the interaction between age and conditions, was affected. Regarding the group comparisons, we found a general increase in brain activation with aging, whereas age-related changes in neurovascular coupling and morphology would cause a reduction in the BOLD response [ 93 ]. Therefore, we assume that such changes did not affect our conclusions, although the age effect may be underestimated.
We hypothesized that the age-related increase in brain activation during single-tasks would result in a reduced residual capacity, causing increased structural interference when performing two tasks simultaneously. Although we found increased brain activation, reduced upregulation from single- to dual-task, and greater DTC in old compared with young adults, we did not find any correlations between the fMRI measures and DTC.
There was no dual-task specific activation in either age group. Therefore, it seems unlikely that the greater DTC in old adults were due to increased structural interference or differences in dual-task specific activation. A promising future research topic is to determine whether processing bottlenecks are present during continuous dual-tasks using high-temporal resolution measures e. Root-mean-square error RMSE angle between the avatar and the vertical during balance and dual-tasking, percentage trials with a correct answer on the calculation task during calculation and dual-tasking, and performance decline from single- to dual-tasking.
Center of pressure CoP velocity during normal standing and root-mean-square error RMSE angle between the avatar and the vertical during simulated standing. Browse Subject Areas? Click through the PLOS taxonomy to find articles in your field. Abstract When two tasks are performed simultaneously, performance often declines in one or both tasks. Introduction Although postural control of standing is highly automated, combining standing with a cognitive task can interfere with the execution of one or both tasks [ 1 ]—[ 4 ].
Download: PPT. Tasks During the balance task, an avatar in the shape of a woman was displayed on the screen. Experimental design An fMRI block-design was used to alternate between the three conditions: balance, calculation, and dual-task. Behavioral data analysis Performance on the balance task was quantified as the root-mean-square error RMSE of the difference in angle between the avatar and its vertical position, averaged across blocks.
DTC was calculated for the balance and calculation tasks using the following formula [ 24 ]: High DTC scores denote a great decline in performance from single- to dual-task. Validity of simulated balance In a separate experiment and subject pool, we determined the validity of balancing the avatar in the supine position in relation to the fluctuation of the center of pressure while standing.
First level fMRI analysis. Group level fMRI analysis. Age effects. Dual-task specific activation. Structural interference. Using the extracted beta values, we calculated the upregulation from single-tasks to dual-task as follows: Mean upregulation was calculated by averaging the upregulation per ROI. Results Behavioral data Fig 2A shows the group data for the performance on the balance task during the balance-only task and balance plus calculation dual-task. Fig 2. Behavioral group data for young and old adults, showing the root-mean-square error RMSE angle between the avatar and the vertical during balance and dual-tasking A , percentage trials with a correct answer on the calculation task during calculation and dual-tasking B , and performance decline from single- to dual-tasking, averaged over the balance and calculation tasks C.
Condition effect on neuroimaging data Table 2 lists the local maxima of activated clusters during balance, calculation and dual-task conditions. Table 2.
Age effect on brain activation Table 3 and Fig 3B display the local maxima of clusters with significantly different activations between young and old adults. Table 3. Dual-task specific activation Table 2 shows that most brain regions involved in dual-tasking are also involved in balance or calculation, suggesting little to no dual-task specific activation. Structural interference A conjunction analysis revealed eight clusters that were activated during both single-tasks in both age groups, including the SMA, right insula, bilateral premotor areas, cerebellum, and parietal lobules Table 4.
Table 4. MNI coordinates and t-values of the local maxima from the conjunction of the balance and calculation contrasts. Fig 4. Fig 5. Scatter plots showing no relationship between the upregulation in BOLD response and the performance decline from single- to dual-tasking in the right insula A and the left parietal lobule B. Table 5.
Behavioral data We consider our dual-task paradigm, comprising calculation plus simulated balancing, challenging and different in nature compared with previous studies that used finger sequencing [ 29 ] or visuomanual drawing and simple mental arithmetic [ 24 ]. Neural correlates of single-tasks Although the condition vs. Increased brain activation in old adults Consistent with previous fMRI studies [ 43 ], [ 62 ]—[ 69 ], old adults exhibited greater brain activation than young adults in all tasks. Dual-task specific activation The literature is inconsistent regarding dual-task specific activation: whereas some studies did find evidence for dual-tasking requiring activation additional to the sum of the single-tasks [ 26 ]—[ 29 ], [ 78 ]—[ 80 ], others did not [ 17 ], [ 24 ], [ 30 ], [ 31 ].
Structural interference Regardless of the functional meaning, we hypothesized that the higher activation in old adults would cause structural interference and therefore greater DTC. Alternative theories As neither structural interference nor dual-task specific activation could explain the age-related deficit in dual-task performance, we must consider alternative theories that could not be tested with the current experimental setup.
Sample size and methodological considerations Low statistical power could underlie the absence of correlations between fMRI measures and DTC.
Professor Nicolas Cherbuin
Conclusions We hypothesized that the age-related increase in brain activation during single-tasks would result in a reduced residual capacity, causing increased structural interference when performing two tasks simultaneously. Supporting information. S1 Appendix. S2 Appendix. Montreal cognitive asessment max. S3 Appendix. Behavioral data. S4 Appendix. S5 Appendix. References 1. Lajoie Y. View Article Google Scholar 2. Riley M. View Article Google Scholar 3. Siu K. View Article Google Scholar 4.
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