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Enhancing vs. inhibiting semantic performance with transcranial magnetic stimulation over the anterior temporal lobe: Frequency- and task-specific effects.

ABSTRACT: Accumulating, converging evidence indicates that the anterior temporal lobe (ATL) appears to be the transmodal hub for semantic representation. A series of repetitive transcranial magnetic stimulation (rTMS) investigations utilizing the 'virtual lesion' approach have established the brain-behavioural relationship between the ATL and semantic processing by demonstrating that inhibitory rTMS over the ATL induced impairments in semantic performance in healthy individuals. However, a growing body of rTMS studies suggest that rTMS might also be a tool for cognitive enhancement and rehabilitation, though there has been no previous exploration in semantic cognition. Here, we explored a potential role of rTMS in enhancing and inhibiting semantic performance with contrastive rTMS protocols (1 Hz vs. 20 Hz) by controlling practice effects. Twenty-one healthy participants were recruited and performed an object category judgement task and a pattern matching task serving as a control task before and after the stimulation over the ATL (1 Hz, 20 Hz, and sham). A task familiarization procedure was performed prior to the experiment in order to establish a 'stable baseline' prior to stimulation and thus minimize practice effect. Our results demonstrated that it is possible to modulate semantic performance positively or negatively depending on the ATL stimulation frequency: 20 Hz rTMS was optimal for facilitating cortical processing (faster RT in a semantic task) contrasting with diminished semantic performance after 1 Hz rTMS. In addition to cementing the importance of the ATL to semantic representation, our findings suggest that 20 Hz rTMS leads to semantic enhancement in healthy individuals and potentially could be used for patients with semantic impairments as a therapeutic tool.

SUBMITTER: Jung J

PROVIDER: S-EPMC8204263 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCognitive impairments are core characteristics of schizophrenia, but are largely resistant to current treatments. Several recent studies have shown that high-frequency repetitive transcranial magnetic stimulation (rTMS) of the left dor-solateral prefrontal cortex (DLPFC) can reduce negative symptoms and improve certain cognitive deficits in schizophrenia patients. However, results are inconsistent across studies.AimTo examine if high-frequency rTMS of the DLPFC can improve visual memory deficits in patients with schizophrenia.MethodsForty-seven chronic schizophrenia patients with severe negative symptoms on stable treatment regimens were randomly assigned to receive active rTMS to the DLPFC (n = 25) or sham stimulation (n = 22) on weekdays for four consecutive weeks. Patients performed the pattern recognition memory (PRM) task from the Cambridge Neuropsychological Test Automated Battery at baseline, at the end of rTMS treatment (week 4), and 4 wk after rTMS treatment (week 8). Clinical symptoms were also measured at these same time points using the Scale for the Assessment of Negative Symptoms (SANS) and the Positive and Negative Syndrome Scale (PANSS).ResultsThere were no significant differences in PRM performance metrics, SANS total score, SANS subscores, PANSS total score, and PANSS subscores between active and sham rTMS groups at the end of the 4-wk treatment period, but PRM performance metrics (percent correct and number correct) and changes in these metrics from baseline were significantly greater in the active rTMS group at week 8 compared to the sham group (all P < 0.05). Active rTMS treatment also significantly reduced SANS score at week 8 compared to sham treatment. Moreover, the improvement in visual memory was correlated with the reduction in negative symptoms at week 8. In contrast, there were no between-group differences in PANSS total score and subscale scores at either week 4 or week 8 (all P > 0.05).ConclusionHigh-frequency transcranial magnetic stimulation improves visual memory and reduces negative symptoms in schizophrenia, but these effects are delayed, potentially due to the requirement for extensive neuroplastic changes within DLPFC networks.

Project description:Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic 'hub' must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of patients with the semantic variant of fronto-temporal lobar degeneration, it has been proposed that this hub is localized within both anterior temporal lobes (ATL), and is functionally connected with verbal 'output' systems via the left ATL. An alternative view, dating from Geschwind's proposal in 1965, is that the angular gyrus (AG) is central to object-based semantic representations. In this fMRI study we examined the connectivity of the left ATL and parietal lobe (PL) with whole brain networks known to be activated during overt picture description. We decomposed each of these two brain volumes into 15 regions of interest (ROIs), using independent component analysis. A dual regression analysis was used to establish the connectivity of each ROI with whole brain-networks. An ROI within the left anterior superior temporal sulcus (antSTS) was functionally connected to other parts of the left ATL, including anterior ventromedial left temporal cortex (partially attenuated by signal loss due to susceptibility artifact), a large left dorsolateral prefrontal region (including 'classic' Broca's area), extensive bilateral sensory-motor cortices, and the length of both superior temporal gyri. The time-course of this functionally connected network was associated with picture description but not with non-semantic baseline tasks. This system has the distribution expected for the production of overt speech with appropriate semantic content, and the auditory monitoring of the overt speech output. In contrast, the only left PL ROI that showed connectivity with brain systems most strongly activated by the picture-description task, was in the superior parietal lobe (supPL). This region showed connectivity with predominantly posterior cortical regions required for the visual processing of the pictorial stimuli, with additional connectivity to the dorsal left AG and a small component of the left inferior frontal gyrus. None of the other PL ROIs that included part of the left AG were activated by Speech alone. The best interpretation of these results is that the left antSTS connects the proposed semantic hub (specifically localized to ventral anterior temporal cortex based on clinical neuropsychological studies) to posterior frontal regions and sensory-motor cortices responsible for the overt production of speech.

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Enhancing vs. inhibiting semantic performance with transcranial magnetic stimulation over the anterior temporal lobe: Frequency- and task-specific effects.

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