The Mind After Midnight: Nocturnal Wakefulness, Behavioral Dysregulation, and Psychopathology

Abstract

Sufficient sleep with minimal interruption during the circadian/biological night supports daytime cognition and emotional regulation. Conversely, disrupted sleep involving significant nocturnal wakefulness leads to cognitive and behavioral dysregulation. Most studies to-date have examined how fragmented or insufficient sleep affects next-day functioning, but recent work highlights changes in cognition and behavior that occur when someone is awake during the night. This review summarizes the evidence for day-night alterations in maladaptive behaviors, including suicide, violent crime, and substance use, and examines how mood, reward processing, and executive function differ during nocturnal wakefulness. Based on this evidence, we propose the Mind after Midnight hypothesis in which attentional biases, negative affect, altered reward processing, and prefrontal disinhibition interact to promote behavioral dysregulation and psychiatric disorders.

Keywords: behavioral dysregulation; circadian rhythms; mental health; nocturnal wakefulness; psychopathology; sleep; substance abuse; suicide.

FIGURE 1

The prevalence and risk for suicide across 24 h. Although most suicides (grey bars, representing % of maximum hourly suicide count) occur around noon, population wakefulness (light grey shaded area) is also maximal at this time and throughout the afternoon and evening. After adjusting for population wakefulness, the incident risk ratio of suicide is substantially increased at night (black line, 95% confidence interval represented by dark grey band), with a 4.25-fold greater risk at 2AM than the 24-h average. Data are derived from the American Time Use Survey and the National Violent Death Reporting System for 2003 to 2010. Data are double-plotted to improve visualization of increased risk during nighttime hours.

FIGURE 2

The Mind after Midnight. Blue boxes on the left and right sides indicate key processes within the model discussed in the text; grey boxes indicate additional components not specifically addressed. During nocturnal wakefulness, upregulation of the amygdala (AMY), nucleus accumbens (NAcc), and the rostral anterior cingulate cortex (rACC) increase emotionally driven salience, attention, and motivation, skew anticipation of risky rewards, and drive excess rumination. Conversely, impairments in the prefrontal cortex (PFC), dorsal anterior cingulate cortex (dACC) and anterior insula (AI) lead to executive dysfunction, diminished cognitive control, and insensitivity to error or loss. These changes promote a cycle of risky behaviors and consequences that can spiral out of control. Figure adapted from Perlis et al. (2016b).