Sustained attention is a limited resource which declines during daily tasks. Such decay is exacerbated in clinical and aging populations. Low-frequency transcranial magnetic stimulation (LF-rTMS) to the intraparietal sulcus (IPS) has potential to upregulate neural activity within the attention network, evidenced by increased activation and functional communication. Attributed to functional compensation for the inhibited node, this boost outlasts the stimulation for tens of minutes. Despite the neural change, no behavioral effect has been found in healthy subjects, a necessary direct evidence of functional compensation. To understand the functional significance of neuromodulatory induced fluctuations on sustained attention, we sought to boost the impact of LF-rTMS through controlling neural excitability prior to LF-rTMS, with the goal to impact behavior. Brain state was controlled using high-frequency transcranial random noise stimulation (HF-tRNS), based on the evidence that HF-tRNS increases and stabilizes neuronal excitability. In male and female human participants, we tested several fMRI-guided stimulation protocols combining HF-tRNS and LF-rTMS. Sustained attention was recorded post-stimulation via a multiple object tracking task (MOT). Whilst attention deteriorated across time in the control condition, HF-tRNS followed by LF-rTMS maintained attention performance up to 94 minutes, doubling the length of successful sustained attention. These results suggest controlling brain state can increase the impact of LF-rTMS in bilateral sustained attention. Used in a cognitive domain dependent on network-wide neural activity, this tool may be effective in causing neural compensation important for clinical rehabilitation.
Significance StatementSustained attention decreases 45 minutes after the onset of a task. Here, we prevent decrement of sustained attention for 94 minutes through applying multi-method brain stimulation. Our stimulation protocol aimed to boost sustained attention through harnessing functional compensation previously found in the attention network following low-frequency rTMS (LF-rTMS) to the IPS, a node of the network. To date, this functional compensation has not provoked behavioral benefit. In our study, controlling brain state with high-frequency transcranial random noise stimulation (HF-tRNS) prior to LF-rTMS resulted in a lasting sustained attention, a crucial effect that could be beneficial to both healthy and clinical populations. Furthermore, given the feasibility of real-world application, this stimulation protocol could be employed ubiquitously to augment cognitive processes.the clinical and healthy populations. Here, we demonstrate attention can be maintained without decrement for up to (and potentially beyond) 94 minutes following multi-method brain stimulation. Future research should be focused on the underlying network changes following multi-method stimulation. Network based compensation for inhibition of one