Neural Substrates of External and Internal Visual Sensations Induced by Human Intracranial Electrical Stimulation

Abstract

Offline perceptions are self-generated sensations that do not involve physical stimulus. These perceptions can be induced by external hallucinated objects or internal imagined objects. However, how the brain dissociates these visual sensations remains unclear. We aimed to map the brain areas involved in internal and external visual sensations induced by intracranial electrical stimulation and further investigate their neural differences. In this study, we collected subjective reports of internal and external visual sensations elicited by electrical stimulation in 40 drug-refractory epilepsy during presurgical evaluation. The response rate was calculated and compared to quantify the dissociated distribution of visual responses. We found that internal and external visual sensations could be elicited when different brain areas were stimulated, although there were more overlapping brain areas. Specifically, stimulation of the hippocampus and inferior temporal cortex primarily induces internal visual sensations. In contrast, stimulation of the occipital visual cortex mainly triggers external visual sensations. Furthermore, compared to that of the dorsal visual areas, the ventral visual areas show more overlap between the two visual sensations. Our findings show that internal and external visual sensations may rely on distinct neural representations of the visual pathway. This study indicated that implantation of electrodes in ventral visual areas should be considered during the evaluation of visual sensation aura epileptic seizures.

Keywords: epilepsy; hippocampus; inferior temporal cortex; intracranial electrical stimulation; offline perception.

FIGURE 1

Cortical distribution of electrodes receiving intracranial electric stimulation. Electrodes were stimulated during the functional mapping sessions over all the patients (n = 40 patients) pooled on the MNI152 brain surface. Blue dots indicate stimulated electrodes, which elicit no visual responses, while red dots indicate stimulated electrodes, which elicit either internal or external visual responses for at least one patient. The structural modules are rendered on the brain’s surface with different colors. dlPFC, dorsal lateral prefrontal cortex; HPC, hippocampus; ITC, inferior temporal cortex; PPC, posterior parietal cortex; and OVC, occipital visual cortex.

FIGURE 2

Internal and external visual sensation probability across the cortical surfaces and structural modules. (A) Mean response probability for internal visual sensations across the cortical surfaces. (B) Mean response probability for external visual sensations across the cortical surface. (C) Normalized response percentage, normalized across modules, for each visual response type. Asterisks indicate regions in which the individual chi-square value exceeds a significant level (p < 0.01, Bonferroni correction for multiple comparisons).

FIGURE 3

Dissociated brain module involvement in involuntary visual imagery and hallucination. (A) Global and module internal visual response percentage. The orange line indicates the average proportion of internal visual responses relative to all the elicited visual responses. The blue line indicates the proportion of internal visual responses within a specific module. (B) Global and module external visual response percentage. The orange line indicates the average proportion of external visual responses relative to all the elicited visual responses. The blue line indicates the proportion of external visual response within a specific module. The dashed black line indicates that the response percentage did not scale linearly for illustration. The modules with a filled large circle exhibit a significantly higher percentage than that of the cortical average (p < 0.01, Binomial test, Bonferroni correction for multiple comparisons).

FIGURE 4

Increased spatial overlap between internal and external visual sensations in regions along the visual processing stream. (A) Spatial Dice coefficient between the internal and external visual sensations at the ROI level rendered on the cortical surface based on a public cytoarchitecture atlas. (B) ROI-based Dice coefficient along visual information processing stream defined generally. Bars indicate the extent of spatial overlap, displayed using the corresponding ROIs color on the above surface. CalcS, calcarine sulcus; FusG, fusiform gyrus; IPL, inferior parietal lobule; IPS, intra-parietal sulcus; LingG, lingual gyrus; LOC, lateral occipital cortex; and STG, superior temporal gyrus.

FIGURE 5

Cross-participant reliability of elicited response to electrical stimulation. (A) Cortical distribution of electrodes that elicited external visual sensation of flickers across different participants. (B) Cortical distribution of electrodes that elicited internal visual sensations by electrical stimulation. Different color-coded dots encode different participants.