Abstract
BackgroundExperiencing emotions engages high-order orbitofrontal and medial prefrontal areas, and expressing emotions involves low-level autonomic structures and peripheral organs. How is information from the cortex transmitted to the periphery? We used two parallel approaches to map simultaneously multiple pathways to determine if hypothalamic autonomic centres are a key link for orbitofrontal areas and medial prefrontal areas, which have been associated with emotional processes, as well as low-level spinal and brainstem autonomic structures. The latter innervate peripheral autonomic organs, whose activity is markedly increased during emotional arousal.ResultsWe first determined if pathways linking the orbitofrontal cortex with the hypothalamus overlapped with projection neurons directed to the intermediolateral column of the spinal cord, with the aid of neural tracers injected in these disparate structures. We found that axons from orbitofrontal and medial prefrontal cortices converged in the hypothalamus with neurons projecting to brainstem and spinal autonomic centers, linking the highest with the lowest levels of the neuraxis. Using a parallel approach, we injected bidirectional tracers in the lateral hypothalamic area, an autonomic center, to label simultaneously cortical pathways leading to the hypothalamus, as well as hypothalamic axons projecting to low-level brainstem and spinal autonomic centers. We found densely distributed projection neurons in medial prefrontal and orbitofrontal cortices leading to the hypothalamus, as well as hypothalamic axonal terminations in several brainstem structures and the intermediolateral column of the spinal cord, which innervate peripheral autonomic organs. We then provided direct evidence that axons from medial prefrontal cortex synapse with hypothalamic neurons, terminating as large boutons, comparable in size to the highly efficient thalamocortical system. The interlinked orbitofrontal, medial prefrontal areas and hypothalamic autonomic centers were also connected with the amygdala.ConclusionsDescending pathways from orbitofrontal and medial prefrontal cortices, which are also linked with the amygdala, provide the means for speedy influence of the prefrontal cortex on the autonomic system, in processes underlying appreciation and expression of emotions.
Highlights
Experiencing emotions engages high-order orbitofrontal and medial prefrontal areas, and expressing emotions involves low-level autonomic structures and peripheral organs
Serial pathways link prefrontal cortices with hypothalamic, spinal, and brainstem autonomic centers We first investigated if pathways that can transmit information from prefrontal cortex to autonomic centers overlap in the hypothalamus with pathways that innervate the lowest autonomic level in the intermediolateral column of the spinal cord
We placed a different retrograde tracer in the intermediolateral column of the thoracic spinal cord (Fig. 1B) to determine if neurons in the hypothalamus project to this spinal autonomic region (Table 1, case AV). This approach indicated that the two pathways overlap in the hypothalamus, demonstrated by intermixing of axonal terminations from the prefrontal pathway, and labeled projection neurons giving rise to the lower pathway leading to the spinal cord
Summary
Experiencing emotions engages high-order orbitofrontal and medial prefrontal areas, and expressing emotions involves low-level autonomic structures and peripheral organs. We used two parallel approaches to map simultaneously multiple pathways to determine if hypothalamic autonomic centres are a key link for orbitofrontal areas and medial prefrontal areas, which have been associated with emotional processes, as well as low-level spinal and brainstem autonomic structures. The latter innervate peripheral autonomic organs, whose activity is markedly increased during emotional arousal. The existence of diverse pathways that underlie emotional processing through the prefrontal cortex in primates has been described in piecemeal fashion in separate studies (for reviews see [15,16,17]) It is not clear if pathways from the prefrontal cortex to autonomic structures are circuitous or relatively direct. These serial pathways may allow direct cortical control of autonomic functions in response to complex emotional situations
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