Zeng et al. offer a fascinating account of how the rise in our body cortisol levels 30-45 min after waking orchestrates a reconfiguration of brain networks underlying working memory, emotional reguation and executive functioning. I pass on the introductory paragraph of the article, followed by the article's abstract. (Motivated readers can obtain a PDF of the entire paper with graphics by emailing me.)
The introductory paragraph:
For centuries, scientists have sought to unravel how the brain and endocrinal signals work in concert to support ever-changing cognitive and environmental demands. In theory, to sustain a dynamic equilibrium between internal milieu and external challenges, the brain and endocrinal signals actively engage in allocation of neural resources to prepare for the upcoming challenges (1, 2). Such active process has been conceptualized as “allostasis” and is believed to serve as one key principle of how neural and endocrinal signals interplay to support nuanced emotional and executive functions, though the underlying mechanisms remain largely elusive. Among endocrinal signals, the stress hormone cortisol plays a critical role in mobilizing energy supply for brain, cognition, and emotion (1, 3, 4). The cortisol awakening response (CAR), in particular, as a natural rise of cortisol through activation of the hypothalamus–pituitary–adrenal (HPA) axis within 30 to 45 min after morning awakening, is superimposed upon the circadian rhythm of cortisol secretion and is more than the mere release of cortisol (5–7). The CAR has been thought to support anticipation of a day’s most reliable stressor—waking up, mobilizing the energy to daily activities (8–10) and proactively modulates human emotion and cognition (11–13). Such proactive effects are reminiscent of a potential mediator of allostasis (1, 14). Although the CAR proactive effects are well documented at a behavioral level, our understanding of the underlying neurobiological mechanisms still remains in its infancy.
The article's abstract:
Emotion and cognition involve an intricate crosstalk of neural and endocrine systems that support dynamic reallocation of neural resources and optimal adaptation for upcoming challenges, an active process analogous to allostasis. As a hallmark of human endocrine activity, the cortisol awakening response (CAR) is recognized to play a critical role in proactively modulating emotional and executive functions. Yet, the underlying mechanisms of such proactive effects remain elusive. By leveraging pharmacological neuroimaging and hidden Markov modeling of brain state dynamics, we show that the CAR proactively modulates rapid spatiotemporal reconfigurations (state) of large-scale brain networks involved in emotional and executive functions. Behaviorally, suppression of CAR proactively impaired performance of emotional discrimination but not working memory (WM), while individuals with higher CAR exhibited better performance for both emotional and WM tasks. Neuronally, suppression of CAR led to a decrease in fractional occupancy and mean lifetime of task-related brain states dominant to emotional and WM processing. Further information-theoretic analyses on sequence complexity of state transitions revealed that a suppressed or lower CAR led to higher transition complexity among states primarily anchored in visual-sensory and salience networks during emotional task. Conversely, an opposite pattern of transition complexity was observed among states anchored in executive control and visuospatial networks during WM, indicating that CAR distinctly modulates neural resources allocated to emotional and WM processing. Our findings establish a causal link of CAR with brain network dynamics across emotional and executive functions, suggesting a neuroendocrine account for CAR proactive effects on human emotion and cognition.