Seeing Scenes: Topographic Visual Hallucinations Evoked by Direct Electrical Stimulation of the Parahippocampal Place Area

Abstract

In recent years, functional neuroimaging has disclosed a network of cortical areas in the basal temporal lobe that selectively respond to visual scenes, including the parahippocampal place area (PPA). Beyond the observation that lesions involving the PPA cause topographic disorientation, there is little causal evidence linking neural activity in that area to the perception of places. Here, we combined functional magnetic resonance imaging (fMRI) and intracranial EEG (iEEG) recordings to delineate place-selective cortex in a patient implanted with stereo-EEG electrodes for presurgical evaluation of drug-resistant epilepsy. Bipolar direct electrical stimulation of a cortical area in the collateral sulcus and medial fusiform gyrus, which was place-selective according to both fMRI and iEEG, induced a topographic visual hallucination: the patient described seeing indoor and outdoor scenes that included views of the neighborhood he lives in. By contrast, stimulating the more lateral aspect of the basal temporal lobe caused distortion of the patient's perception of faces, as recently reported (Parvizi et al., 2012). Our results support the causal role of the PPA in the perception of visual scenes, demonstrate that electrical stimulation of higher order visual areas can induce complex hallucinations, and also reaffirm direct electrical brain stimulation as a tool to assess the function of the human cerebral cortex.

Mapping human brain networks with cortico-cortical evoked potentials

“…Recently, optogenetics have allowed the selective stimulation of neuronal subtypes in localized regions of animal brains [40] and assessing the effects of that stimulation on functional neural networks [41]. With the increasing use of research protocols to study effects of cortical stimulation in patients implanted with invasive electrodes for epilepsy monitoring, there has been recent resurgence of interest into the effects of cortical stimulation upon behaviour and perception [26,[42][43][44]. While most of the aforementioned work focused on the link between stimulation and changes in perception or behaviour (e.g.…”

“…There is a rich history of this [35,109], and more recent observations include: (i) high-frequency stimulation of the entorhinal cortex improving spatial memory [27], (ii) experiential phenomena occuring only when electrical stimulation of visual cortex is associated with activity in the temporo-parietal junction [26], (iii) electrical stimulation of the anterior cingulate cortex eliciting the will to persevere [44] and (iv) stimulation to the right inferior frontal cortex inducing more slowing when motor braking was required in a go-no-go task [28,42]. Other studies examined the electrophysiological effects of electrical stimulation during rest, thus without assessing behaviour [52].…”

Clarifying the Role of Neural Networks in Complex Hallucinatory Phenomena

“…Although Mégevand et al (2014) reveal a direct role for PPA activity in complex hallucinations and déjà vu, such localized activity does not explain the entire spectrum of hallucinatory experiences. For instance, hallucinatory phenomena are known to occur in response to neural stimulation in extra-temporal regions and in clinical disorders characterized by extra-temporal lobe dysfunction.…”

“…The PPA is historically defined as the posterior subregion of the parahippocampal cortex, although more recent evidence confirms peak activation for scene-selective processing can extend to the lateral edge of the collateral sulcus, adjacent to the medial fusiform gyrus (Nasr et al, 2011). Mégevand et al (2014) demonstrate a direct link between the PPA and topographic hallucinations, thereby providing evidence of a role for PPA neuronal activity in conscious scene perception. Importantly, their work further confirms the significance of the parahippocampal region in complex visual hallucinations and déjà vu.…”

“…This comparison may explain why chronic visual hallucinations in schizophrenia and Parkinson's disease, which are associated with more diffuse pathology, can often become increasingly vivid and difficult to separate from reality. Considering the findings of Mégevand et al (2014) in such a framework highlights that pathological complex hallucinatory experiences are best considered a network phenomenon.…”