Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network - PubMed (original) (raw)

Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network

Saskia Haegens et al. Hum Brain Mapp. 2010 Jan.

Abstract

Successful working memory (WM) requires the engagement of relevant brain areas but possibly also the disengagement of irrelevant areas. We used magnetoencephalography (MEG) to elucidate the temporal dynamics of areas involved in a somatosensory WM task. We found an increase in gamma band activity in the primary and secondary somatosensory areas during encoding and retention, respectively. This was accompanied by an increase of alpha band activity over task-irrelevant regions including posterior and ipsilateral somatosensory cortex. Importantly, the alpha band increase was strongest during successful WM performance. Furthermore, we found frontal gamma band activity that correlated both with behavioral performance and the alpha band increase. We suggest that somatosensory gamma band activity reflects maintenance and attention-related components of WM operations, whereas alpha band activity reflects frontally controlled disengagement of task-irrelevant regions. Our results demonstrate that resource allocation involving the engagement of task-relevant and disengagement of task-irrelevant regions is needed for optimal task execution.

2009 Wiley-Liss, Inc.

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Figures

Figure 1

Figure 1

Experimental design of the somatosensory delayed‐match‐to‐sample memory task. The sample consisted of a series of pulses (7–10 Hz) and was always presented to the right hand; the probe was 1 Hz slower or faster than the corresponding sample and presented either to the right or left hand. Subjects had to indicate whether the probe stimulus was of higher or lower frequency than the sample.

Figure 2

Figure 2

Oscillatory activity during the probe presentation. (a) Topographic plot showing an increase in gamma band activity (40–80 Hz) over contralateral somatosensory sensors during probe presentation (t = 3–4 s). Sensors showing significant increase (P < 0.01) are marked with asterisks. (b) Topographic plot showing a decrease in alpha and beta band activity (10–30 Hz) over contralateral somatosensory sensors during probe presentation (t = 3–4 s). Sensors showing significant decrease (P < 0.05) are marked with asterisks. (c, d) Sagittal (left), coronal (middle) and axial (right) slices showing gamma (c) and alpha/beta power (d) source reconstructions obtained using beamforming. Sources of somatosensory gamma and alpha/beta activity are located in primary sensorimotor cortex (Brodmann areas 3, 4). All plots are showing power as log ratio of probe right versus probe left, grand‐averaged over 18 subjects.

Figure 3

Figure 3

Gamma band activity during the retention interval. (a) Topographic plot showing a sustained increase in high gamma band activity (100–150 Hz) over bilateral somatosensory sensors during the retention interval (t = 1–3 s) as compared to baseline (t = −1–0 s). Sensors showing significant effects (P < 0.01) are marked with asterisks. (b) Average TFR of the somatosensory channels identified in (a), showing sustained increase of broadband gamma activity during the retention interval as compared to baseline. Stimulus artifacts can be observed at t = 0–1 and t = 3–4 s (scale as in a). (c) Sagittal (left), coronal (middle) and axial (right) slices showing gamma power source reconstructions obtained using beamforming. Sustained somatosensory gamma activity is presumably located in bilateral SII. (d) Sagittal (left), coronal (middle) and axial (right) slices showing sustained somatosensory gamma activity in bilateral SII in one subject. All plots are showing power as log ratio of retention versus baseline, grand‐averaged over 18 subjects (except for d).

Figure 4

Figure 4

Gamma band activity modulated by task performance. (a) Topographic plot showing higher gamma band activity (65–80 Hz) for correct than for incorrect trials, over frontal sensors during the retention interval (t = 1–3 s). Sensors showing a trend (P = 0.08) are marked with a circle. (b) Average TFR of the channels identified in (a), showing higher gamma activity for correct than for incorrect trials, during the retention interval (scale as in a). (c) Sagittal (left), coronal (middle) and axial (right) slices showing gamma power source reconstructions obtained using beamforming. Frontal gamma activity is mainly located in superior frontal gyrus. (d) Graph showing subject performance (% correct) versus average frontal gamma power (difference of the gamma power for correct versus incorrect trials). Each point represents one subject. Frontal gamma power correlates significantly with task performance (Spearman r = 0.474, P < 0.05). All plots are showing power as log ratio of correct versus incorrect trials, grand‐averaged over 18 subjects.

Figure 5

Figure 5

Alpha band activity during the retention interval. (a) Topographic plot showing an increase in alpha band activity (8–14 Hz) over posterior sensors during the retention interval (t = 1–3 s) as compared to baseline (t = −1–0 s). Sensors showing significant effect (P < 0.05) are marked with asterisks. (b) Average TFR of the posterior channels identified in (a), showing sustained increase of alpha activity during the retention interval as compared to baseline (scale as in a). (c) Sagittal (left), coronal (middle) and axial (right) slices showing alpha power source reconstructions obtained using beamforming. Posterior alpha activity is located in occipital cortex (including Brodmann areas 17, 18, 19). All plots are showing power as log ratio of retention versus baseline, grand‐averaged over 18 subjects.

Figure 6

Figure 6

Alpha band activity modulated by task performance. (a) Topographic plot showing higher alpha band activity (8–14 Hz) for correct than for incorrect trials, over posterior and right lateralized sensors during the early retention interval (t = 1–2 s). Sensors showing significant effect (P < 0.05) are marked with asterisks. (b) Average TFR of the channels identified in (a), showing higher alpha activity for correct than for incorrect trials, during the early retention interval (scale as in a). (c) Sagittal (left), coronal (middle) and axial (right) slices showing alpha power source reconstructions obtained using beamforming. Alpha activity is distributed over visual and right lateralized regions. (d) Graph showing alpha power versus frontal gamma power (both averaged over previously identified channels and frequency bands during the retention interval, difference of the power for correct versus incorrect trials). Each point represents one subject. Frontal gamma power correlates significantly with alpha power (Spearman r = 0.509, P < 0.05). All plots are showing power as log ratio of correct versus incorrect trials, grand‐averaged over 18 subjects.

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