Emotion and the Cardiovascular System: Postulated Role of Inputs From the Medial Prefrontal Cortex to the Dorsolateral Periaqueductal Gray

Abstract

The midbrain periaqueductal gray (PAG) plays a major role in generating different types of behavioral responses to emotional stressors. This review focuses on the role of the dorsolateral (dl) portion of the PAG, which on the basis of anatomical and functional studies, appears to have a unique and distinctive role in generating behavioral, cardiovascular and respiratory responses to real and perceived emotional stressors. In particular, the dlPAG, but not other parts of the PAG, receives direct inputs from the primary auditory cortex and from the secondary visual cortex. In addition, there are strong direct inputs to the dlPAG, but not other parts of the PAG, from regions within the medial prefrontal cortex that in primates correspond to cortical areas 10 m, 25 and 32. I first summarise the evidence that the inputs to the dlPAG arising from visual, auditory and olfactory signals trigger defensive behavioral responses supported by appropriate cardiovascular and respiratory effects, when such signals indicate the presence of a real external threat, such as the presence of a predator. I then consider the functional roles of the direct inputs from the medial prefrontal cortex, and propose the hypothesis that these inputs are activated by perceived threats, that are generated as a consequence of complex cognitive processes. I further propose that the inputs from areas 10 m, 25 and 32 are activated under different circumstances. The input from cortical area 10 m is of special interest, because this cortical area exists only in primates and is much larger in the brain of humans than in all other primates.

Keywords: Brodmann cortical area 10; cardiovascular regulation; cognition; defensive behavior; medial prefrontal cortex; periaqueductal gray; respiratory activity.

Figure 1

Schematic diagram showing major inputs to the dlPAG and the proposed output pathways subserving the co-ordinated changes in sympathetic vasomotor and respiratory activity regulated by the dlPAG. The lines with arrows indicate connections, that could be either direct (monosynaptic) or indirect (polysynaptic). Other abbreviations: CnF, cuneiform nucleus; DMH, dorsomedial hypothalamus; lPAG, lateral part of the periaqueductal gray. Modified from Dampney et al. (2013).

Figure 2

(A) Sagittal midline section of the human brain showing the location of cortical areas 10 m, 25 and 32. (B) Relative density of labeled axonal terminals in the dorsomedial (dm), dorsolateral (dl), lateral (l), and ventrolateral (vl) parts of the PAG, following injection of anterograde tracer into areas 10 m, 25 and 32 in the medial prefrontal cortex of the macaque. Modified from An et al. (1998), with permission; (C) Example of distribution of labeled terminals in the PAG and surrounding areas following injection of anterograde tracer into areas 10 m in one experiment. The location of the area on the right is indicated by the rectangle over a standard section of the midbrain on the left. Modified from An et al. (1998). (D) Relative volumes of area 10 m in different primate species, expressed both as an absolute measure (in ml) or relative measure (% of brain volume). Modified from Semendeferi et al. (2001), with permission.