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Stimulation of the left dorsolateral prefrontal cortex with slow rTMS enhances verbal memory formation.

ABSTRACT: Encoding of episodic memories relies on stimulus-specific information processing and involves the left prefrontal cortex. We here present an incidental finding from a simultaneous EEG-TMS experiment as well as a replication of this unexpected effect. Our results reveal that stimulating the left dorsolateral prefrontal cortex (DLPFC) with slow repetitive transcranial magnetic stimulation (rTMS) leads to enhanced word memory performance. A total of 40 healthy human participants engaged in a list learning paradigm. Half of the participants (N = 20) received 1 Hz rTMS to the left DLPFC, while the other half (N = 20) received 1 Hz rTMS to the vertex and served as a control group. Participants receiving left DLPFC stimulation demonstrated enhanced memory performance compared to the control group. This effect was replicated in a within-subjects experiment where 24 participants received 1 Hz rTMS to the left DLPFC and vertex. In this second experiment, DLPFC stimulation also induced better memory performance compared to vertex stimulation. In addition to these behavioural effects, we found that 1 Hz rTMS to DLPFC induced stronger beta power modulation in posterior areas, a state that is known to be beneficial for memory encoding. Further analysis indicated that beta modulations did not have an oscillatory origin. Instead, the observed beta modulations were a result of a spectral tilt, suggesting inhibition of these parietal regions. These results show that applying 1 Hz rTMS to DLPFC, an area involved in episodic memory formation, improves memory performance via modulating neural activity in parietal regions.

SUBMITTER: van der Plas M

PROVIDER: S-EPMC8478201 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundTreating memory and cognitive deficits requires knowledge about anatomical sites and neural activities to be targeted with particular therapies. Emerging technologies for local brain stimulation offer attractive therapeutic options but need to be applied to target specific neural activities, at distinct times, and in specific brain regions that are critical for memory formation.MethodsThe areas that are critical for successful encoding of verbal memory as well as the underlying neural activities were determined directly in the human brain with intracranial electrophysiological recordings in epilepsy patients. We recorded a broad range of spectral activities across the cortex of 135 patients as they memorised word lists for subsequent free recall.FindingsThe greatest differences in the spectral power between encoding subsequently recalled and forgotten words were found in low theta frequency (3-5 Hz) activities of the left anterior prefrontal cortex. This subsequent memory effect was proportionally greater in the lower frequency bands and in the more anterior cortical regions. We found the peak of this memory signal in a distinct part of the prefrontal cortex at the junction between the Broca's area and the frontal pole. The memory effect in this confined area was significantly higher (Tukey-Kramer test, p<0.05) than in other anatomically distinct areas.InterpretationOur results suggest a focal hotspot of human verbal memory encoding located in the higher-order processing region of the prefrontal cortex, which presents a prospective target for modulating cognitive functions in the human patients. The memory effect provides an electrophysiological biomarker of low frequency neural activities, at distinct times of memory encoding, and in one hotspot location in the human brain.FundingOpen-access datasets were originally collected as part of a BRAIN Initiative project called Restoring Active Memory (RAM) funded by the Defence Advanced Research Project Agency (DARPA). CT, ML, MTK and this research were supported from the First Team grant of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund.

Project description:BackgroundThe left dorsolateral prefrontal cortex (DLPFC) is involved in early-phase manual dexterity skill acquisition when cognitive control processes, such as integration and complexity demands, are required. However, the effectiveness of left DLPFC transcranial direct current stimulation (tDCS) on early-phase motor learning and whether its effectiveness depends on the cognitive demand of the target task are unclear. This study aimed to investigate whether tDCS over the left DLPFC improves non-dominant hand dexterity performance and determine if its efficacy depends on the cognitive demand of the target task.MethodsIn this randomized, double-blind, sham-controlled trial, 70 healthy, right-handed, young adult participants were recruited. They were randomly allocated to the active tDCS (2 mA for 20 min) or sham groups and repeatedly performed the Purdue Pegboard Test (PPT) left-handed peg task and left-handed assembly task three times: pre-tDCS, during tDCS, and post tDCS.ResultsThe final sample comprised 66 healthy young adults (mean age, 22.73 ± 1.57 years). There were significant interactions between group and time in both PPT tasks, indicating significantly higher performance of those in the active tDCS group than those in the sham group post tDCS (p < 0.001). Moreover, a greater benefit was observed in the left-handed assembly task performance than in the peg task performance (p < 0.001). No significant correlation between baseline performance and benefits from tDCS was observed in either task.ConclusionsThese results demonstrated that prefrontal tDCS significantly improved early-phase manual dexterity skill acquisition, and its benefits were greater for the task with high cognitive demands. These findings contribute to a deeper understanding of the underlying neurophysiological mechanisms of the left DLPFC in the modulation of early-phase dexterity skill acquisition.Trial registrationThis study was registered in the University Hospital Medical Information Network Clinical Trial Registry in Japan (UMIN000046868), Registered February 8, 2022 https://center6.umin.ac.jp/cgi-open-bin/ctr_e/ctr_view.cgi?recptno=R000053467.

Project description:Conflict adaptation is a hallmark effect of adaptive cognitive control and refers to the adjustment of control to the level of previously experienced conflict. Conflict monitoring theory assumes that the dorsolateral prefrontal cortex (DLPFC) is causally involved in this adjustment. However, to date, evidence in humans is predominantly correlational, and heterogeneous with respect to the lateralization of control in the DLPFC. We used high-definition transcranial direct current stimulation (HD-tDCS), which allows for more focal current delivery than conventional tDCS, to clarify the causal involvement of the DLPFC in conflict adaptation. Specifically, we investigated the regional specificity and lateralization of potential beneficial stimulation effects on conflict adaptation during a visual flanker task. One hundred twenty healthy participants were assigned to four HD-tDCS conditions: left or right DLPFC or left or right primary motor cortex (M1). Each group underwent both active and sham HD-tDCS in crossover, double-blind designs. We obtained a sizeable conflict adaptation effect (measured as the modulation of the flanker effect as a function of previous response conflict) in all groups and conditions. However, this effect was larger under active HD-tDCS than under sham stimulation in both DLPFC groups. In contrast, active stimulation had no effect on conflict adaptation in the M1 groups. In sum, the present results indicate that the DLPFC plays a causal role in adaptive cognitive control, but that the involvement of DLPFC in control is not restricted to the left or right hemisphere. Moreover, our study confirms the potential of HD-tDCS to modulate cognition in a regionally specific manner. SIGNIFICANCE STATEMENT:Conflict adaptation is a hallmark effect of adaptive cognitive control. While animal studies have suggested causal involvement of the DLPFC in this phenomenon, such evidence is currently lacking in humans. The present study used high-definition transcranial direct current stimulation (HD-tDCS) to demonstrate that the DLPFC is causally involved in conflict adaptation in humans. Our study confirms a central claim of conflict monitoring theory, which up to now has predominantly relied on correlational studies. Our results further indicate an equal involvement of the left and right DLPFC in adaptive control, whereas stimulation of a control region-the primary motor cortex-had no effect on adaptive control. The study thus confirms the potential of HD-tDCS to modulate cognition in a regionally specific manner.

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Stimulation of the left dorsolateral prefrontal cortex with slow rTMS enhances verbal memory formation.

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