Intensity of affective experience is modulated by magnitude of intracranial electrical stimulation in human orbitofrontal, cingulate and insular cortices

Abstract

The subjective and behavioral effects of intracranial electrical stimulation (iES) have been studied for decades, but there is a knowledge gap regarding the relationship between the magnitude of electric current and the type, intensity and valence of evoked subjective experiences. We report on rare iES data from 18 neurosurgical patients with implanted intracranial electrodes in the orbitofrontal cortex (OFC), the insula (INS) and the anterior portion of cingulate cortex (ACC). ACC stimulation elicited somatic and visceral sensations, whereas OFC stimulation predominantly elicited olfactory and gustatory responses, and INS stimulation elicited a mix of effects involving somatic and visceral sensations, olfaction and gustation. Further, we found striking evidence that the magnitude of electric current delivered intracranially correlated positively with the perceived intensity of subjective experience and the evoked emotional state, a relationship observed across all three regions. Finally, we observed that the majority of reported experiences were negatively valenced and unpleasant, especially those elicited by ACC stimulation. The present study provides novel case studies from the human brain confirming that these structures contribute causally to the creation of affective states and demonstrates a direct relationship between the magnitude of electrical stimulation of these structures and the qualia of elicited subjective experience. Summary: This study provides critical knowledge about the effect of electrical charge magnitude on the intensity of human subjective experiences and emotional states. We shed light on the fundamental relationship between the electrical (physical) state of cortical tissue and the modality and intensity of human (subjective) experience. As electroceutical interventions are increasingly employed to treat neurological and psychiatric disorders, these findings highlight the importance of electrical stimulation magnitude for eliciting specific changes in human subjective experience.

Insula and Olfaction: A Literature Review and Case Report

“…Electrocortical stimulation studies of the insular cortex have reported olfactory responses which show some similarities to our case. Notably, these studies reported that stimulation of the insula more often causes unpleasant olfactory sensations [43][44][45]. Our patient described the unpleasant smell as resembling decay and rot, in line with parosmia.…”

“…Responses elicited by electrical stimulation of the insular cortex, in patients with epilepsy undergoing neurosurgery, provide additional crucial information on the role of the insula in sensory processing. Olfactory sensations following electrical stimulation of the insula have been described as "something funny (...), like medicine, a sickly smell" [43] and unpleasant [44,45], in line with the notion of phantosmia. It should be noted, however, that olfactory sensations represent only 1% of responses to electrical stimulation of the insular cortex and are concentrated around the central insular sulcus [44], while most responses are somatosensory and visceral sensations.…”

Does the Prefrontal Cortex Play an Essential Role in Consciousness? Insights from Intracranial Electrical Stimulation of the Human Brain

“…Expanding on this work showing that iES of OFC and ACC can elicit profound effects on consciousness, Yih et al (2019) explored whether the intensity of changes in conscious experience was linked to the magnitude of the electrical stimulation itself. First, they replicated prior work showing that ACC stimulation elicited changes primarily in the visceral and somatic domains, while stimulation to the OFC elicited changes chiefly in olfactory experience.…”

“…Further, there is wide variability in the stimulation parameters and electrode types used by different research groups, and the busy inpatient hospital setting of iES research seldom allows for a comprehensive exploration of this parameter space. This is critical because the effects elicited by iES are known to vary with the frequency and amplitude of stimulation (Mohan et al, 2020), with higher parameter values tending to elicit more potent responses across many domains, including visual (Winawer and Parvizi, 2016;Bosking et al, 2017), physiological (Inman et al, 2018), and emotional effects (Yih et al, 2019). Additionally, research throughout the early-tomid 20th century tended to use monopolar stimulation (as do most DBS interventions today), whereas bipolar stimulation is the standard in most contemporary iES functional mapping sessions.…”

Minimal functional alignment of ventromedial prefrontal cortex intracranial EEG signals during naturalistic viewing

“…Prior intracranial work investigating the vmPFC has relied on more traditional task-based paradigms to characterize its role in computing value [47][48][49][50] . Stimulation paradigms have implicated the involvement of the vmPFC in the subjective experience of affect, olfaction, and gustation 51,52 . Naturalistic designs, such as passive movie watching, can provide rich contextual information, which makes them well suited for studying social, cognitive, and affective processes [53][54][55] , but have been rarely used in intracranial EEG research 56,57 .…”