Intrinsic Organization and Function of Human Brain Networks Supporting the Spontaneous Dynamics of Attention and Pain

Abstract

The intrinsic dynamics of human brain activity enable us to flexibly shift our attention between the external environment and cognition unrelated to immediate sensation. The interplay of stimulus-dependent and stimulus-independent experience characterizes the nature of our personal interactions with the world and differences among individuals. Brain networks involved in attention, sensory modulation, and stimulus-independent cognition have been described. The present work was designed to disentangle how these networks are intrinsically organized and how fluctuating activity in these networks relates to cognition and a basic perception that is fundamental for survival, pain. The salience/ventral attention network, implicated in stimulus-driven attention, was shown to exhibit right hemisphere-lateralized intrinsic organization, both in structural and functional connectivity. The default mode network (DMN), implicated in attention away from the external environment, was shown to have dynamic fluctuations in the functional organization of its subnetworks that relate to ongoing, freely flowing thoughts (mind-wandering). In the context of pain, activity in multiple networks was associated with spontaneous attentional fluctuations. Attention toward pain was represented as increased salience/ventral network activation. Attention away from pain occurred during increased DMN activation and enhanced functional connectivity between the DMN and periaqueductal gray (PAG), a key node of the descending pain modulatory system. Furthermore, individuals with higher tendency to mind-wander away from pain exhibited stronger PAG-DMN structural connectivity and more dynamic PAG-DMN spontaneous functional connectivity. These findings underscore the behavioural significance of activity fluctuations within attention and sensory modulation networks. While activity in these networks is constrained by structural and functional properties that underlie inter-individual differences, it is also highly flexible and tracks attentional fluctuations toward and away from the present sensory environment. This work has implications for understanding of pathological states such as chronic pain, where altered activity dynamics in attention/antinociceptive networks may determine disease prognosis and therapeutic outcomes.