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Altered alpha and theta oscillations correlate with sequential working memory in Parkinson's disease.

ABSTRACT: Daily activities such as preparing a meal rely on the ability to arrange thoughts and actions in the right order. Patients with Parkinson's disease have difficulties in sequencing tasks. Their deficits in sequential working memory have been associated with basal ganglia dysfunction. Here we demonstrate that altered parietal alpha and theta oscillations correlate with sequential working memory in Parkinson's disease. We included 15 patients with Parkinson's disease (6 women, mean age: 66.0 years), 24 healthy young (14 women, mean age: 24.1 years), and 16 older participants (7 women, mean age: 68.6 years). All participants completed a picture ordering task with scalp electroencephalogram (EEG) recording, where they arranged five pictures in a specific order and memorized them over a delay. When encoding and maintaining picture sequences, patients with Parkinson's disease showed a lower baseline alpha peak frequency with higher alpha power than healthy young and older participants. Patients with a higher baseline alpha power responded more slowly for ordered trials. When manipulating picture sequences, patients with Parkinson's disease showed a lower frequency of maximal power change for random versus ordered trials than healthy young and older participants. Healthy older participants showed a higher frequency of maximal power change than healthy young participants. Compared with patients with frequency of maximal power change in the alpha band (8-15 Hz), patients with frequency of maximal power change in the theta band (4-7 Hz) showed a higher ordering-related accuracy cost (random versus ordered) in the main task and tended to respond more slowly and less accurately in an independent working memory test. In conclusion, altered baseline alpha oscillations and task-dependent modulation of alpha and theta oscillations may be neural markers of poor sequential working memory in Parkinson's disease.

SUBMITTER: Ye Z

PROVIDER: S-EPMC9214782 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Maintaining and manipulating sequences online is essential for daily activities such as scheduling a day. In Parkinson's disease (PD), sequential working memory deficits have been associated with altered regional activation and functional connectivity in the basal ganglia. This study demonstrates that the substantia nigra (SN) integrity correlated with basal ganglia function and sequencing performance in 29 patients with PD (17 women) and 29 healthy controls (HC, 18 women). In neuromelanin-sensitive structural MRI, PD patients showed smaller SN than HC. In a digit ordering task with functional MRI, participants either recalled sequential digits in the original order ('pure recall') or rearranged the digits and recalled the new sequence ('reorder & recall'). PD patients performed less accurately than HC, accompanied by the caudate and pallidal hypo-activation, subthalamic hyper-activation, and weakened functional connectivity between the bilateral SN and all three basal ganglia regions. PD patients with larger SN tended to exhibit smaller ordering-related accuracy costs ('reorder & recall' versus 'pure recall'). This effect was fully mediated by the ordering-related caudate activation. Unlike HC, the ordering-related accuracy cost correlated with the ordering-related caudate activation but not subthalamic activation in PD. Moreover, the ordering-related caudate activation correlated with the SN area but not the daily dose of D2/3 receptor agonists. In PD, the daily dose of D2/3 receptor agonists correlated with the ordering-related subthalamic activation, which was not related to the accuracy cost. The findings suggest that damage to the SN may lead to sequential working memory deficits in PD, mediated by basal ganglia dysfunction.SIGNIFICANCELiu et al. demonstrate that damage to the substantia nigra (SN) correlates with basal ganglia dysfunction and poor sequencing performance in Parkinson's disease (PD). In neuromelanin-sensitive MRI, PD showed smaller SN than healthy controls. In a digit ordering task with functional MRI, PD's lower task accuracy was accompanied by the caudate and pallidal hypo-activation, subthalamic hyper-activation, and weakened functional connectivity between the SN and basal ganglia. PD with larger SN exhibited greater ordering-related caudate activation and lower ordering-related accuracy cost when sequencing digits. PD with more daily exposure to D2/3 receptor agonists exhibited greater ordering-related subthalamic activation, which did not reduce accuracy cost. It suggests that the SN may affect sequencing performance by regulating the task-dependent caudate activation in PD.

Project description:BackgroundFrontal midline theta (FMT) oscillations (4-8 Hz) are strongly related to cognitive and executive control during mental tasks such as memory processing, arithmetic problem solving or sustained attention. While maintenance of temporal order information during a working memory (WM) task was recently linked to FMT phase, a positive correlation between FMT power, WM demand and WM performance was shown. However, the relationship between these measures is not well understood, and it is unknown whether purposeful FMT phase manipulation during a WM task impacts FMT power and WM performance. Here we present evidence that FMT phase manipulation mediated by transcranial alternating current stimulation (tACS) can block WM demand-related FMT power increase (FMT?power) and disrupt normal WM performance.MethodsTwenty healthy volunteers were assigned to one of two groups (group A, group B) and performed a 2-back task across a baseline block (block 1) and an intervention block (block 2) while 275-sensor magnetoencephalography (MEG) was recorded. After no stimulation was applied during block 1, participants in group A received tACS oscillating at their individual FMT frequency over the prefrontal cortex (PFC) while group B received sham stimulation during block 2. After assessing and mapping phase locking values (PLV) between the tACS signal and brain oscillatory activity across the whole brain, FMT power and WM performance were assessed and compared between blocks and groups.ResultsDuring block 2 of group A but not B, FMT oscillations showed increased PLV across task-related cortical areas underneath the frontal tACS electrode. While WM task-related FMT?power and WM performance were comparable across groups in block 1, tACS resulted in lower FMT?power and WM performance compared to sham stimulation in block 2.ConclusiontACS-related manipulation of FMT phase can disrupt WM performance and influence WM task-related FMT?power. This finding may have important implications for the treatment of brain disorders such as depression and attention deficit disorder associated with abnormal regulation of FMT activity or disorders characterized by dysfunctional coupling of brain activity, e.g., epilepsy, Alzheimer's or Parkinson's disease (AD/PD).

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Altered alpha and theta oscillations correlate with sequential working memory in Parkinson's disease.

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