Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease

Abstract

The brain is the key organ of stress reactivity, coping, and recovery processes. Within the brain, a distributed neural circuitry determines what is threatening and thus stressful to the individual. Instrumental brain systems of this circuitry include the hippocampus, amygdala, and areas of the prefrontal cortex. Together, these systems regulate physiological and behavioral stress processes, which can be adaptive in the short-term and maladaptive in the long-term. Importantly, such stress processes arise from bidirectional patterns of communication between the brain and the autonomic, cardiovascular, and immune systems via neural and endocrine mechanisms underpinning cognition, experience, and behavior. In one respect, these bidirectional stress mechanisms are protective in that they promote short-term adaptation (allostasis). In another respect, however, these stress mechanisms can lead to a long-term dysregulation of allostasis in that they promote maladaptive wear-and-tear on the body and brain under chronically stressful conditions (allostatic load), compromising stress resiliency and health. This review focuses specifically on the links between stress-related processes embedded within the social environment and embodied within the brain, which is viewed as the central mediator and target of allostasis and allostatic load.

Figures

Figure 1

Schematic illustration of the location and key functions of limbic brain areas that play an integrated role in cognitive, emotional, and visceral control processes important for allostasis, allostatic load, and stress responding. Each of the three brain areas is discussed in detail in the text in relation to both animal model studies that focus on what happens at the cellular and molecular levels and studies on the human brain using functional and structural imaging and neuropsychological and neuroendocrine assessments.

Figure 2

Neurobiological pathways of SES and allostatic load. A heuristic schematic illustrating the potential neurobiological pathways by which psychosocial factors related to SES may impact allostatic control systems underpinning allostatic load and disease risk. In childhood and adolescence, psychosocial factors related to SES and reviewed elsewhere in this volume (e.g., parental resources and education) are likely to interact with genetic and dispositional individual differences to affect the neuroplasticity of limbic brain areas that regulate allostatic control systems. These brain areas include subdivisions of the prefrontal cortex (e.g., the anterior cingulate cortex in purple), hippocampus (in blue-green), and the amygdala (in red). Importantly, these limbic areas regulate neuroendocrine, autonomic, and immune systems, which are involved in the bidirectional allodynamic control of central and peripheral physiology. In adulthood and later life, psychosocial factors related to SES (e.g., meaningful employment and social integration) may similarly interact with individual difference and behavioral lifestyle factors to affect the neuroplasticity and aging of the same limbic systems mediating and targeted by allostatic control systems. To the extent that lower SES adversely affects limbic neuroplasticity via stress-related factors, then the regulation of key allostatic control systems may become impaired, leading to allostatic load on the body and brain and perhaps increased risk for ill health.

Figure 3

Lower perceived parental social standing predicted greater amygdala reactivity to angry faces in a functional neuroimaging study of young adults. (A) Social ladders used to assess perceived parental social standing. (B) Statistical parametric maps projected onto an anatomical template. The maps profile amygdala areas where lower perceived parental social standing predicted greater reactivity to angry faces. (C) Plots depicting standardized perceived parental social standing scores (x-axis) and mean-centered, standardized reactivity values derived from left (L, open circles, dashed line) and right (R, closed circles, solid line) amygdala areas in B. Inset in C illustrates exemplar trial of angry faces used to elicit amygdala reactivity. From Gianaros et al. (2008), reprinted with permission.

Figure 4

Lower subjective social status, as reflected by a lower self-reported ranking on a “social ladder”, was associated with reduced gray matter volume in the perigenual area of the anterior cingulate cortex (pACC). (A) Illustration of 10-point social ladder scale used to assess subjective social status. (B) Overlaid on an anatomical template is a statistical parametric map of color-scaled t-values, which illustrate the pACC area where lower subjective social status was associated with reduced gray matter volume across individuals. (C) Plotted along the y-axis is the standardized (z-score) gray matter volume values for pACC area profiled in B. Plotted along the x-axis are social ladder rankings from the scale illustrated in A (1 = “Worst Off,” 10 = “Best Off”). *P < 0.001. From Gianaros et al. (2007), reprinted with permission.