A neural correlate of visceral emotional responses: evidence from fMRI of the thoracic spinal cord. Soc Cogn Affect Neurosci

Abstract

Functional magnetic resonance imaging (fMRI) of thoracic spinal cord neurons was used to examine the neural correlates of visceral emotional responses. Participants completed four spinal fMRI runs involving passive viewing (i.e. no movement) and motoric responses to negative or neutral images. Negative images, particularly in the movement condition, elicited robust activity in motoric nuclei, indicating action preparedness. These images also enhanced activity in autonomic and sensory nuclei, thus providing a clear neural representation of visceral responses to emotional stimuli. Keywords: magnetic resonance imaging; functional MRI; spinal cord; thoracic spinal cord; emotion A core feature of emotional experience is a subjective visceral response to a stimulus or event. These responses imbue events with a vividness that enhances perception Quantifying neural activity related to such phenomenologically complex experiences poses significant methodological challenges. Paramount among these is the difficulty in separating neural activity related to the bodily responses from activity associated with the cognitive interpretation of these responses. Previous research has successfully identified key structures related to the latter. Activation of the right insula has been consistently linked with interoception One such region is the spinal cord, which has different sensory, motoric and autonomic functions but is not directly related to any cognitive process. The spinal cord is divided into four different regionscervical, thoracic, lumbar and sacraleach of which is composed of a number of individual segments projecting to and receiving information from different regions of the body. Each of these segments consists of dorsal and ventral aspects, which correspond to sensory and motoric activity and, in the thoracic segments, a lateral aspect that corresponds to autonomic activity. Although often thought to be a simple structure, the patterns of activity in the spinal cord reflect a number of potentially interacting systems. Numerous separate descending pathways from the brain modulate motoric regions of the spinal cord, and similarly, multiple separate ascending pathways bring different types of somatosensory information back to the brain. In addition to these brain-spinal cord interactions, the spinal cord houses interneurons that project both intra-segmentally and intersegmentally and that are involved in a number of reflexive responses that occur independent of the brain. Therefore, studies examining the excitability of a single descending pathway from the brain (e.g. the corticospinal tract) are measuring only a fraction of the activity occurring in the spinal cord. Examining activity at the level of the spinal cord itself will provide researchers with unique information about nervous system activity that cannot be identified using traditional brain fMRI (functional magnetic resonance imaging). In previous studies, we have used fMRI of the spinal cord ('spinal fMRI'; Stroman, 2005) to examine whether the spinal cord activity can be modulated by emotional stimuli. In the first study to examine spinal cord responses to emotions, we measured activity in the cervical spinal cord, which innervates the upper limbs including the hands (Smith and Kornelsen, 2011). We found that negative emotional stimuli elicited greater levels of activity in ventral (motoric) regions of several spinal cord segments, particularly those related to hand responses. This activity was more pronounced when participants made a movement (pressed a button on a response pad) than when they passively viewed the emotional images. Because of this very specific pattern of activity, we suggested that spinal cord neurons show evidence of emotion-dependent 'action preparedness'. However, emotional responses are obviously not limited to rapid gestural responses, as shown by measurements of the cervical spinal cord. Instead, emotional responses generally involve muscle tension in the chest and abdomen as well as autonomic nervous system activity. Neuroanatomical studies suggest that these responses should be linked with activity in a different region of the spinal cord, the thoracic cord. Spinal nerves emanating from the thoracic spinal cord innervate muscles in the trunk and abdomen, stimulating muscle contraction of these regions. Afferent somatosensory projections from the peripheral nervous system synapse with this region as well. These responses are likely linked to the subjective awareness of our emotionally aroused state. Additionally, the thoracic spinal cord is critical for a number of autonomic nervous system responses ranging from pupil dilation and cardiopulmonary responses (segments T1-T4) to the secretion of norepinephrine and epinephrine by the adrenal medulla (T10-T12; see Shields, 1993, for a detailed review). Therefore, measuring activit