Concurrent TMS-fMRI Reveals Interactions between Dorsal and Ventral Attentional Systems

Abstract

Adaptive behavior relies on combining bottom-up sensory inputs with top-down control signals to guide responses in line with current goals and task demands. Over the past decade, accumulating evidence has suggested that the dorsal and ventral frontoparietal attentional systems are recruited interactively in this process. This fMRI study used concurrent transcranial magnetic stimulation (TMS) as a causal perturbation approach to investigate the interactions between dorsal and ventral attentional systems and sensory processing areas. In a sustained spatial attention paradigm, human participants detected weak visual targets that were presented in the lower-left visual field on 50% of the trials. Further, we manipulated the presence/absence of task-irrelevant auditory signals. Critically, on each trial we applied 10 Hz bursts of four TMS (or Sham) pulses to the intraparietal sulcus (IPS). IPS-TMS relative to Sham-TMS increased activation in the parietal cortex regardless of sensory stimulation, confirming the neural effectiveness of TMS stimulation. Visual targets increased activations in the anterior insula, a component of the ventral attentional system responsible for salience detection. Conversely, they decreased activations in the ventral visual areas. Importantly, IPS-TMS abolished target-evoked activation increases in the right temporoparietal junction (TPJ) of the ventral attentional system, whereas it eliminated target-evoked activation decreases in the right fusiform. Our results demonstrate that IPS-TMS exerts profound directional causal influences not only on visual areas but also on the TPJ as a critical component of the ventral attentional system. They reveal a complex interplay between dorsal and ventral attentional systems during target detection under sustained spatial attention.

Significance statement: Adaptive behavior relies on combining bottom-up sensory inputs with top-down attentional control. Although the dorsal and ventral frontoparietal systems are key players in attentional control, their distinct contributions remain unclear. In this TMS-fMRI study, participants attended to the left visual field to detect weak visual targets presented on half of the trials. We applied brief TMS bursts (or Sham-TMS) to the dorsal intraparietal sulcus (IPS) 100 ms after visual stimulus onset. IPS-TMS abolished the visual induced response suppression in the ventral occipitotemporal cortex and the response enhancement to visual targets in the temporoparietal junction. Our results demonstrate that IPS causally influences neural activity in the ventral attentional system 100 ms poststimulus. They have important implications for our understanding of the neural mechanisms underlying attentional control.

Keywords: detection; interleaved/concurrent TMS-fMRI; multisensory; neglect; right parietal cortex; spatial attention.