Using a Developmental Ecology Framework to Align Fear Neurobiology Across Species

Abstract

Children's development is largely dependent on caregiving; when caregiving is disrupted, children are at increased risk for numerous poor outcomes, in particular psychopathology. Therefore, determining how caregivers regulate children's affective neurobiology is essential for understanding psychopathology etiology and prevention. Much of the research on affective functioning uses fear learning to map maturation trajectories, with both rodent and human studies contributing knowledge. Nonetheless, as no standard framework exists through which to interpret developmental effects across species, research often remains siloed, thus contributing to the current therapeutic impasse. Here, we propose a developmental ecology framework that attempts to understand fear in the ecological context of the child: their relationship with their parent. By referring to developmental goals that are shared across species (to attach to, then, ultimately, separate from the parent), this framework provides a common grounding from which fear systems and their dysfunction can be understood, thus advancing research on psychopathologies and their treatment.

Keywords: development; ecology; fear; human; parental buffering; rodent; stress.

Figure 1

(a) Graphical depiction of cross-species alignment of fear learning and the relevant neural circuits across typical maturation within the developmental ecology framework. (b) Summary of fear learning circuitry across the three phases of typical development in early life for rodents (i–iii) and humans (iv–vi). Gray shading indicates the presumed functional maturity of different structures based on the evidence. Functional connectivity in humans is depicted by lines connecting structures, and the presumed maturity of those structures is illustrated by whether the line is solid (mature) or broken (immature). The same scheme is used for rodent connectivity, with the additional complexity of indicating whether the connection is an excitatory (triangle) or inhibitory (perpendicular) projection, a distinction afforded by the greater specificity of the evidence from rodents. Abbreviations: HPC, hippocampus; IL, infralimbic region of the PFC; LC, locus coeruleus; OB, olfactory bulb; Pir, piriform cortex; PFC, prefrontal cortex; PL, prelimbic region of the PFC; PND, postnatal day.

Figure 2

Select rodent models of early caregiving adversities discussed in this review. The fear behavior and circuitry that have been associated with these early caregiving adversities are listed under the heading Outcome, and the developmental ecology phase at which those outcomes have been reported is listed under Phase. Abbreviations: HPA, hypothalamic–pituitary–adrenal; LA, lateral amygdala; PFC, prefrontal cortex.