Neural-heart interactions in the healthy and injured brain

Banellis, Leah ORCID: 0000-0002-1911-1830 (2022). Neural-heart interactions in the healthy and injured brain. University of Birmingham. Ph.D.

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Abstract

Introduction
Integrating internal and external signals is fundamental for perceiving and interacting with the world via the body. In particular, interoceptive predictive coding frameworks describe these integrated mechanisms as vital for embodied selfhood, emotional experience, and a unified first-person perspective. By definition, a disorder of consciousness patient has dysfunctional awareness of their self and their environment. Despite the dual diagnostic criteria, research has focused almost exclusively on external perceptual awareness, leaving internal self-related aspects of awareness largely unexplored. Thus, we sought to detect neural markers of self-related interoceptive processing with the aim that their detection may predict the recovery of self-awareness in acute unresponsive disorders of consciousness.
Experiment one
First, we aimed to identify neural markers of interoceptive (i.e., cardiac) and exteroceptive (i.e., auditory) integration in healthy individuals. We presented sequences of sounds at a short delay (i.e., perceived synchronous) or long delay (i.e., perceived asynchronous) from the heartbeat, with half the trials including an omission. We analysed heart-evoked potentials (i.e., HEPs) during omissions to measure pure predictive mechanisms without contaminating auditory responses. Pre-omission HEP responses differed across short delay and long delay trials, potentially reflecting differences in heartbeat-driven expectations of sounds. Furthermore, attending to internal heartbeat sensations modulated omission-evoked responses, supporting the role of attentional-precision in regulating cross-modal predictive mechanisms (i.e., state precision). However, we did not observe modulation of HEP/omission-evoked responses by individual difference in interoceptive ability, which doesn't support the proposed regulating role of trait precision in predictive coding frameworks. Therefore, HEP mechanisms of interoceptive and exteroceptive integration operate partially under interoceptive predictive coding. However, we observed inconsistent evidence of modulation by precision-weighting.
Experiment two
Second, we sought to determine whether the lack of observed trait precision modulation (i.e., by interoceptive ability) and, therefore, inconsistency with precision- weighting resulted from individual differences in the perceived timing of heartbeat sensations. Thus, in experiment two, we tailored the perceived synchronous cardio-audio delays to each individual to test the influence of trait precision more sensitively. Despite this, we observed no significant modulation of HEPs by state or trait precision. Nonetheless, we replicated the robust HEP effect indicative of cardio-audio expectation. Thus, overall, our findings are inconsistent with a precision-weighted predictive coding view. However, it could be that participants relied less on attentional/state precision under a more individually-tailored task. Furthermore, assessing interoceptive ability is challenging, and thus, our interoceptive performance measures may not accurately reflect trait precision.
Experiment three
Finally, cortical processing of heartbeats at rest is thought to index self-related aspects of awareness, such as embodied selfhood and the formation of a first-person perspective. Hence, we investigated the prognostic potential of resting HEPs and cardiac measures in acute unresponsive patients. We observed no convincing evidence of HEPs or cardiac measures predicting recovery from acute unresponsiveness, three or six months post-assessment. This lack of evidence suggests resting HEPs are not useful for consciousness prognoses. However, greater prognostic value may be found in HEPs during high-level self-processing or interoceptive-exteroceptive integration (i.e., Experiments one and two).
Discussion
In summary, we observed robust HEP evidence of interoceptive signals guiding expectations of exteroceptive stimuli. However, we observed inconsistent evidence of modulation of HEPs by state precision and no evidence of modulation by trait precision. Thus, we need more explicit definitions of the manipulation and measurement of precision in predictive coding frameworks to test their influence on interoceptive predictive mechanisms accurately. Finally, although previous evidence indicated the diagnostic value of HEPs, we observed no convincing evidence of their prognostic potential. It is possible that during rest, self-cognitive mechanisms reflected in HEPs are reduced. Therefore, investigating HEPs during tasks involving high-level self-processing or interoceptive-exteroceptive integration may be more valuable for awareness prognoses.

Type of Work:

Thesis (Doctorates > Ph.D.)

Award Type:

Doctorates > Ph.D.

Supervisor(s):