Attention in Space and Time: From Behavior to Neural Mechanisms

Abstract

In the human brain, visual attention has been predominantly studied using methods with high spatial, but poor temporal resolution such as fMRI, or high temporal, but poor spatial resolution such as EEG/MEG. We investigated the temporal dynamics and attention effects across the human visual system at a mesoscopic level that combines precise spatial and temporal measurements by using electrocorticography in epilepsy patients performing a spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system, thereby relating them to topography and processing hierarchy. We demonstrate regional differences in temporal dynamics and modulatory effects of spatial attention across the visual processing hierarchy. Our findings only partially support attentional top-down models that promote influences on visual cortex by reversing the processing hierarchy. Further, we explored the neural underpinnings of selective attention involved in target enhancement and distractor suppression. Whether these two aspects engage similar or divergent cortical neuronal populations, and how they are implemented in the human visual system to map spatial attention remain unclear. We characterized the cortical distribution and temporal dynamics of alpha-band oscillations, demonstrating a spatiotemporal dissociation between population neural activities engaged in target enhancement and distractor suppression during the deployment of spatial attention. We also found that interareal communication is enhanced through cross-frequency interactions along the visual hierarchy to facilitate the processing of a spatially predictable target. In contrast, sensory processing and interareal communication are suppressed through local cross-frequency modulation to attenuate the processing of potential distractors. Our findings reveal that such a distributed cortical organization and complementary neural mechanisms enable efficient gating and filtering of sensory information in the anticipatory processing of spatial attention. In addition to visual spatial attention, we also probed auditory temporal attention and examined its modulatory effect on temporal expectation using structured sound sequences with varied predictability. We observed an improved behavioral performance in healthy subjects when detecting targets embedded in a predictable temporal structure. We also found that target detection was enhanced for the attended sequence while attenuated for the unattended sequence, with an additional facilitation derived from fast adaptive theta entrainment.