Multimodal neurocognitive markers of interoceptive tuning in smoked cocaine

Abstract

Contemporary neurocognitive models of drug addiction have associated this condition with changes in interoception-namely, the sensing and processing of body signals that fulfill homeostatic functions relevant for the onset and maintenance of addictive behavior. However, most previous evidence is inconsistent, behaviorally unspecific, and virtually null in terms of direct electrophysiological and multimodal markers. To circumvent these limitations, we conducted the first assessment of the relation between cardiac interoception and smoked cocaine dependence (SCD) in a sample of (a) 25 participants who fulfilled criteria for dependence on such a drug, (b) 22 participants addicted to insufflated clorhidrate cocaine (only for behavioral assessment), and (c) 25 healthy controls matched by age, gender, education, and socioeconomic status. We use a validated heartbeat-detection (HBD) task and measured modulations of the heart-evoked potential (HEP) during interoceptive accuracy and interoceptive learning conditions. We complemented this behavioral and electrophysiological data with offline structural (MRI) and functional connectivity (fMRI) analysis of the main interoceptive hubs. HBD and HEP results convergently showed that SCD subjects presented ongoing psychophysiological measures of enhanced interoceptive accuracy. This pattern was associated with a structural and functional tuning of interoceptive networks (reduced volume and specialized network segregation). Taken together, our findings provide the first evidence of an association between cardiac interoception and smoked cocaine, partially supporting models that propose hyper-interoception as a key aspect of addiction. More generally, our study shows that multimodal assessments of interoception could substantially inform the clinical and neurocognitive characterization of psychophysiological and neurocognitive adaptations triggered by addiction.

At the Heart of Neurological Dimensionality: Cross-Nosological and Multimodal Cardiac Interoceptive Deficits

“…For a) HBD behavioral results, mean distance accuracy was the best predictor, confirming previous comparisons of different indexes ( 29 ). This metric presents advantages to capture ongoing and temporally subtle adaptations across the task ( 18 , 78 ). Moreover, cardiac interoceptive accuracy proves more sensitive than cardiac interoceptive learning ( 10 , 13 , 30 ) across cardiac and neurological conditions.…”

“…Data were collected between January 2014 and July 2017. The study was approved by the ethics committee of the Institute of Cognitive Neurology as part of an ongoing protocol ( 9 , 10 , 13 , 17 , 18 , 43 ). All participants provided informed consent in accordance with the Declaration of Helsinki, and the study was carried out observing the privacy rights of human participants and in line with the Recommendations for the Conduct, Reporting, Editing and Publication of Scholarly Work in Medical Journals ( 44 ).…”

“…To control for individual differences in heart rate (HR), each tapped response was time-locked to the ECG R-peak based on three different time windows: 750 milliseconds after the beat for an HR less than 69.76 beats/min, 600 milliseconds after the beat for an HR between 69.75 and 94.25 beats/min, and 400 milliseconds after the beat for an HR higher than 94.25 beats/min. The third cardiac interoceptive metric, mean distance accuracy, estimates the synchronization between motor responses and corresponding heartbeats ( 17 , 18 ). This index evaluates the synchronization between heartbeats and associated motor responses.…”

“…HBD tasks allow for tapping multiple cardiac interoceptive dimensions across varied levels of analyses in healthy and neurological samples ( 10 , 12 , 16 , 17 ). Behaviorally, this task yields measures of interoceptive accuracy (the ability to correctly monitor each heartbeat), sensibility (subjective impressions of one’s own interoceptive performance), learning (improvement of behavioral accuracy after auditory feedback), and awareness (metacognitive assessments of one’s own interoceptive skills) ( 10 , 18 ). Neurophysiologically, cardiac interoceptive processes are indexed by the heart-evoked potential (HEP) ( 19 – 24 ), a cortical marker modulated by conscious attention to heartbeats ( 10 , 13 , 20 , 25 ).…”

Multicentric evidence of emotional impairments in hypertensive heart disease

“…Interoceptive performance was assessed through a modified version of a validated heartbeat detection task 29 , 59 – 64 , in which patients are asked to attend to their own heartbeats (see Fig. 2 A and Supplementary Material C.).…”