The Brainstem in Emotion: A Review

Abstract

Emotions depend upon the integrated activity of neural networks that modulate arousal, autonomic function, motor control, and somatosensation. Brainstem nodes play critical roles in each of these networks, but prior studies of the neuroanatomic basis of emotion, particularly in the human neuropsychological literature, have mostly focused on the contributions of cortical rather than subcortical structures. Given the size and complexity of brainstem circuits, elucidating their structural and functional properties involves technical challenges. However, recent advances in neuroimaging have begun to accelerate research into the brainstem's role in emotion. In this review, we provide a conceptual framework for neuroscience, psychology and behavioral science researchers to study brainstem involvement in human emotions. The "emotional brainstem" is comprised of three major networks - Ascending, Descending and Modulatory. The Ascending network is composed chiefly of the spinothalamic tracts and their projections to brainstem nuclei, which transmit sensory information from the body to rostral structures. The Descending motor network is subdivided into medial projections from the reticular formation that modulate the gain of inputs impacting emotional salience, and lateral projections from the periaqueductal gray, hypothalamus and amygdala that activate characteristic emotional behaviors. Finally, the brainstem is home to a group of modulatory neurotransmitter pathways, such as those arising from the raphe nuclei (serotonergic), ventral tegmental area (dopaminergic) and locus coeruleus (noradrenergic), which form a Modulatory network that coordinates interactions between the Ascending and Descending networks. Integration of signaling within these three networks occurs at all levels of the brainstem, with progressively more complex forms of integration occurring in the hypothalamus and thalamus. These intermediary structures, in turn, provide input for the most complex integrations, which occur in the frontal, insular, cingulate and other regions of the cerebral cortex. Phylogenetically older brainstem networks inform the functioning of evolutionarily newer rostral regions, which in turn regulate and modulate the older structures. Via these bidirectional interactions, the human brainstem contributes to the evaluation of sensory information and triggers fixed-action pattern responses that together constitute the finely differentiated spectrum of possible emotions.

Keywords: brainstem; emotion; feeling; interoception; medulla; midbrain; networks; pons.

FIGURE 1

Brainstem nuclei involved in human emotion. (A) Sagittal view and (B) Coronal view. DR, Dorsal Raphe; LC, Locus coeruleus; LDT, Laterodorsal tegmental nucleus; Mb, Midbrain; MR, Median raphe; P, Pons; PAG, Periaqueductal gray; PBC, Parabrachial nuclear complex; PPN, Pedunculopontine nucleus; VTA, Ventral tegmental area. The substantia nigra and the nucleus of the tractus solitarius are not shown to optimize visibility of the other structures.

FIGURE 2

Major structures involved in the Ascending network. (1) Spinothalamic tracts. (2) Nucleus of the tractus solitarius. (3) Parabrachial nuclear complex. (4) Thalamus. Green arrows: Ascending projections.

FIGURE 3

Holstege’s conception of the Emotional and Somatic motor systems. (Adapted from Holstege, 2016).

FIGURE 4

Major structures involved in the Descending network. (5) Periaqueductal gray. (6) Locus coeruleus. (7) Caudal raphe nuclei. (8) Rostral ventrolateral medullary nuclei. (9) Dorsal motor nucleus of the vagus nerve. Green arrows: Descending projections from periaqueductal gray. Blue arrows: Descending projections from the caudal raphe and locus coeruleus.

FIGURE 5

The nuclei of the Modulatory network. (10) Substantia nigra. (11) Ventral tegmental area. (12) Raphe nuclei. (6) Locus coeruleus. (13) Pedunculopontine nucleus. (14) Laterodorsal tegmental nucleus.