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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.

SUBMITTER: Yih J

PROVIDER: S-EPMC6537947 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Synaptic dysfunction in schizophrenia may be associated with abnormal expression or function of soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins (syntaxin, synaptosomal-associated protein 25 [SNAP25], vesicle-associated membrane protein [VAMP]) forming the molecular complex underlying neurosecretion. The impact of such abnormalities on efficient SNARE heterotrimer formation is poorly understood. We investigated putative SNARE dysfunction, along with possible roles for the SNARE binding partners Munc18-1, complexins (Cplx) 1/2, and synaptotagmin in brains from autopsies of individuals with and without schizophrenia.Postmortem samples were obtained from orbitofrontal cortex (OFC) and/or anterior cingulate cortex from two separate cohorts (n = 15 + 15 schizophrenia cases, n = 13 + 15 control subjects). SNARE interactions were studied by immunoprecipitation and one- or two-dimensional blue native polyacrylamide gel electrophoresis (BN-PAGE).In the first cohort, syntaxin, Munc18-1, and Cplx1, but not VAMP, Cplx2, or synaptotagmin, were twofold enriched in SNAP25 immunoprecipitated products from schizophrenia OFC in the absence of any alterations in total tissue homogenate levels of these proteins. In BN-PAGE, the SNARE heterotrimer was identified as a 150-kDa complex, increased in schizophrenia samples from cohort 1 (OFC: +45%; anterior cingulate cortex: +44%) and cohort 2 (OFC: +40%), with lower 70-kDa SNAP25-VAMP dimer (-37%) in the OFC. Upregulated 200-kDa SNARE-Cplx1 (+65%) and downregulated 550-kDa Cplx1-containing oligomers (-24%) in schizophrenia OFC were identified by BN-PAGE. These findings were not explained by postmortem interval, antipsychotic medication, or other potentially confounding variables.The findings support the hypothesis of upregulated SNARE complex formation in schizophrenia OFC, possibly favored by enhanced affinity for Munc18-1 and/or Cplx1. These alterations offer new therapeutic targets for schizophrenia.

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

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