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

Jeyoung Jung,Matthew A Lambon Ralph

doi:10.1016/j.neuroimage.2021.117959

Jeyoung Jung, Matthew A Lambon Ralph

Open Access

https://doi.org/10.1016/j.neuroimage.2021.117959

Copy DOI

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.

Highlights

Concepts and meaning are fundamental components of human cognition
A crucial form of convergent evidence for the causal role of the anterior temporal lobe (ATL) in semantic representation came through a series of experiments with healthy participants using repetitive transcranial magnetic stimulation demonstrating that rTMS over the ATL causes transient impairments in various semantic tasks (Pobric G et al 2007; Lambon Ralph MA et al 2009; Pobric G et al 2009; Binney RJ et al 2010; Pobric G, E Jefferies and MA Lambon Ralph 2010; Pobric G, E Jefferies and MA Ralph 2010; Jackson RL et al 2015; Jung J and MA Lambon Ralph 2016)
Having selected 20Hz rTMS from the pilot study, we investigated its effects on semantic performance in comparison to an opposing, inhibitory stimulation (1 Hz) and sham stimulation

Summary

Introduction

Concepts and meaning are fundamental components of human cognition. We use this knowledge every day to recognise objects in our environment, to anticipate how they will behave and interact with each other and, use them to perform functions, to generate expectations for situations, and to interpret language. A crucial form of convergent evidence for the causal role of the ATL in semantic representation came through a series of experiments with healthy participants using repetitive transcranial magnetic stimulation (rTMS) demonstrating that rTMS over the ATL causes transient impairments in various semantic tasks (Pobric G et al 2007; Lambon Ralph MA et al 2009; Pobric G et al 2009; Binney RJ et al 2010; Pobric G, E Jefferies and MA Lambon Ralph 2010; Pobric G, E Jefferies and MA Ralph 2010; Jackson RL et al 2015; Jung J and MA Lambon Ralph 2016) This ‘virtual lesion’ rTMS approach has been useful to verify brain-behaviour relationships, several studies have shown enhancement in cognitive performance, suggesting that rTMS is capable of facilitating cortical activity at the site of simulation (for a review, see Vallar G and N Bolognini 2011), depending on the type and frequency of stimulation (Miniussi C and PM Rossini 2011). We tested various rTMS protocols for enhancing vs diminishing semantic processing

Methods

Results

Conclusion