Controlling Brain State Prior to Stimulation of Parietal Cortex Prevents Deterioration of Sustained Attention.

Grace Edwards,Loryn K Bucci,Federica Contò,Lorella Battelli

doi:10.1093/texcom/tgaa069

Abstract

Sustained attention is a limited resource which declines during daily tasks. Such decay is exacerbated in clinical and aging populations. Inhibition of the intraparietal sulcus (IPS), using low-frequency repetitive transcranial magnetic stimulation (LF-rTMS), can lead to an upregulation of functional communication within the attention network. Attributed to functional compensation for the inhibited node, this boost lasts for tens of minutes poststimulation. Despite the neural change, no behavioral correlate has been found in healthy subjects, a necessary direct evidence of functional compensation. To understand the functional significance of neuromodulatory induced fluctuations on attention, we sought to boost the impact of LF-rTMS to impact behavior. We controlled brain state prior to LF-rTMS using high-frequency transcranial random noise stimulation (HF-tRNS), shown to increase and stabilize neuronal excitability. Using fMRI-guided stimulation protocols combining HF-tRNS and LF-rTMS, we tested the poststimulation impact on sustained attention with multiple object tracking (MOT). While attention deteriorated across time in control conditions, HF-tRNS followed by LF-rTMS doubled sustained attention capacity to 94 min. Multimethod stimulation was more effective when targeting right IPS, supporting specialized attention processing in the right hemisphere. Used in cognitive domains dependent on network-wide neural activity, this tool may cause lasting neural compensation useful for clinical rehabilitation.

Highlights

Sustained attention is fundamental for cognitively interacting with the environment (DeGangi & Porges, 1990), it progressively deteriorates over time (Sarter et al, 2001; Berardi et al, 2001; Whitehurst et al, 2019)
We examined the effect of multi-method non-invasive brain stimulation on bilateral attention, dependent of visual field
When computing contrasts on estimated marginal means, we found a significant difference in tracking performance at 80-94 minutes between the left visual field contralateral to tRNS & rTMS to right intraparietal sulcus (IPS) and control (estimate = 0.572, se = 0.138, zratio = 4.157, p=0.0006; emmeans(), with adjust ”mvt”)

Summary

Introduction

Sustained attention is fundamental for cognitively interacting with the environment (DeGangi & Porges, 1990), it progressively deteriorates over time (Sarter et al, 2001; Berardi et al, 2001; Whitehurst et al, 2019). One hypothesis is that network-wide functional change compensates for the inhibited node following LF-rTMS (Paus et al, 1997; Grefkes et al, 2009; Lee & D’Esposito, 2012; Plow et al, 2014; Battelli et al, 2017). Lee & D’Esposito (2012) found theta burst TMS to prefrontal cortex (PFC) increased connectivity in the unstimulated PFC homologue which correlated with a reduced disruption of working memory Such behavioral correlate in attention has not been found following network-wide lasting functional changes after LF-rTMS to IPS in healthy participants (Plow et al, 2014; Battelli et al, 2017). Enduring behavioral change is crucial for non-invasive brain stimulation to be considered in clinical intervention (Edwards et al, 2019)

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