A shared theta-rhythmic process for selective sampling of environmental information and internally stored information

Abstract

Selective attention is the collection of mechanisms through which the brain preferentially processes behaviorally important information. Many everyday tasks, such as shopping for groceries, require selective sampling (i.e., attention-related sampling) of both external information (i.e., information from the environment) and internally stored information (i.e., information being maintained in working memory). While there is clear evidence that selective sampling of external information is influenced by internally stored information (and vice versa), the extent to which selective sampling of external and internal information share neural resources remains a focus of debate. Previous research has linked theta-rhythmic (3-8 Hz) neural activity in higher-order (e.g., frontal cortices) and sensory regions to theta-rhythmic changes in behavioral performance during selective sampling. Here, we used EEG and a dual-task design (i.e., a task that required both external and internal information), in male and female humans, to directly compare theta-dependent fluctuations in behavioral performance during external sampling with those during internal sampling. Our findings are consistent with a shared theta-rhythmic process for selectively sampling external information or internal information. This theta-rhythmic sampling is associated with both phase-dependent changes in sensory responses (i.e., as measured with the N1 component) and phase-dependent changes in interactions between external and internal information. The theta phase associated with weaker sensory responses and relatively worse behavioral performance (i.e., the bad phase) is also associated with a slowed perceptual decision-making process (as measured with the CPP component), specifically during dual-task trials when to-be-detected external information matches to-be-remembered internal information. SIGNIFICANCE STATEMENTMost everyday tasks require information from both the external environment and internal memory stores; however, the extent to which selective processing of external and internal information rely on shared neural mechanisms and resources remains a subject of debate. Recent work has demonstrated attention-related, theta-rhythmic fluctuations (3-8 Hz) in neural activity and behavioral performance, perhaps reflecting the temporal coordination of competing functions (e.g., attention-related sampling and shifting). Here, we used EEG and a dual-task design to provide evidence of a shared, theta-rhythmic process for alternately boosting the sampling of either external or internal information. This shared, theta-rhythmic process also modulates interactions between external and internal information on dual-task trials, when these sources of information compete for limited processing resources.