Single neurons in thalamus and subthalamic nucleus process cardiac and respiratory signals in humans

Abstract

Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: Ventral Intermedius nucleus (Vim) and Ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. We observed neurons with increases or decreases in firing rate in response to either the heartbeat or the inter-beat interval. Peaks of neural activity were found at different phases of the cardiac and respiratory cycles. Whereas most neurons only responded to one of the tested signals, a substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. By extensively describing for the first time single unit activity related to cardiorespiratory function in thalamic and subthalamic neurons, our results highlight the major role of these subcortical regions in the processing of visceral signals.

Emotional state as a modulator of autonomic and somatic nervous system activity in postural control: a review

“…Within the body, these responses involve endocrine, autonomic, and musculoskeletal responses ( 19 ). Furthermore, autonomic activity, such as increased respiration or heart rate, has a direct modulatory effect on the activity of the thalamic nuclei (i.e., changing their firing rate) and this may have implications for the way sensory and motor information is processed and/or relayed by the thalamus to other regions of the cortex and subcortical areas during emotional responses ( 53 ). This has direct implications for postural control because if the gain of somatosensory processing has been altered, it will result in a change in response to a given stimulus, such as loss of balance.…”

“…These studies highlight the relationship between emotional state and postural control in quiet stance that may be amplified in more challenging conditions such as reduced vision. One explanation for the altered sensory utilization could be due to the fact that the chronic increased sympathetic activation that is present in those with higher trait relative anxiety, as well as during state anxiety (i.e., situational specific “stress-response”/increased arousal), both mediated by the RF/RAS, thalamus and hypothalamus, leads to changes in sensory processing and subsequent changes in sensory-motor responses ( 53 ). As mentioned earlier in this review, this has direct implications for postural control because if the gain of somatosensory processing has been altered, it will result in a change in response to a given stimulus (i.e., loss of balance or challenge to the balance system).…”

“…Those individuals who experienced the feeling of fear of falling during the study had a corresponding change to their motor control as well as alterations in sensory feedback. Autonomic responsivity (e.g., increased respiration or heart rate) that may occur in individuals who experience fear when standing at the edge of an elevated platform, can have a direct modulatory effect on the activity of the thalamic nuclei and this has implications for the way sensory information is processed and/or relayed by the thalamus to other regions of the cortex and subcortical areas ( 53 ). From this perspective, it is possible that participants in the Ellmers study who interpreted the behaviours indicative of “postural stiffening” as potentially harmful, also had more pronounced shifts in utilisation of sensory feedback, resulting in altered interpretation of the incoming sensory information (demonstrating how cognitive-emotional state impacts behavioural outcomes).…”