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Articles, Behavioral/Cognitive

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

Pierre Mégevand, David M. Groppe, Matthew S. Goldfinger, Sean T. Hwang, Peter B. Kingsley, Ido Davidesco and Ashesh D. Mehta
Journal of Neuroscience 16 April 2014, 34 (16) 5399-5405; DOI: https://doi.org/10.1523/JNEUROSCI.5202-13.2014
Pierre Mégevand
1Departments of Neurosurgery, Feinstein Institute for Medical Research,
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David M. Groppe
1Departments of Neurosurgery, Feinstein Institute for Medical Research,
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Matthew S. Goldfinger
1Departments of Neurosurgery, Feinstein Institute for Medical Research,
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Sean T. Hwang
2Neurology, and
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Peter B. Kingsley
3Radiology, Hofstra North Shore-LIJ School of Medicine, Manhasset, New York 11030, and
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Ido Davidesco
4Neuroscience Institute, Princeton University, Princeton, New Jersey 08540
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Ashesh D. Mehta
1Departments of Neurosurgery, Feinstein Institute for Medical Research,
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    Figure 1.

    Location of the intracranial electrodes, house-specific visual responses identified by fMRI, iEEG, and results of electrical brain stimulation. A, The location of the intracranial electrodes of shafts DTIp and DHb is displayed on the patient's high-resolution T1 MRI. Inset, Illustration of the coronal slices along the rostral-caudal axis. All DTIp electrodes were in the same coronal plane. For DHb, contacts 4 and 3 were on the coronal slice located in the inset; contacts 6 and 5 were on the coronal slice immediately rostral; and contacts 2 and 1 on the slice immediately caudal. The white arrow highlights the collateral sulcus; white arrowhead, the occipitotemporal sulcus. B, Regions that displayed greater BOLD responses to houses than other visual stimuli are overlaid on the patient's isometric axial T1 MRI. The basal temporal electrodes DHb and DTIp are also displayed. The inset shows a coronal slice in the plane of DTIp. The effect of direct electrical stimulation of pairs of neighboring electrodes is depicted as colored circles, or stars if there were afterdischarges as a result of the stimulation. The color codes for the symbols are detailed in C. The axial slice shown was in the plane of contacts DTIp5 through 2 and of contacts DHb4 and 3. DTIp7 and 1 and DHb6 and 5 were on the slice immediately (1 mm) dorsal and were projected down; DTIp8 was 2 mm dorsal and was also projected down; DHb2 and 1 were 1 mm ventral and were projected up. C, Left, Exemplars of stimuli used in iEEG paradigm to detect visual category-selective cortex. The fMRI paradigm included houses, faces, tools and patterns but not body parts. Right, Color codes for the symbols used to summarize the results of electrical stimulation in B and D (see Results; Table 1). D, Event-related changes in iEEG broadband gamma/high gamma power (40–160 Hz) following presentation of five categories of images. Different categories are represented by different colors (C). Shading indicates SE. Black dotted lines below each plot indicate significantly (padj < 0.01) higher responses to places than other visual stimuli. Gray lines indicate significantly (padj < 0.01) higher responses to faces than other visual stimuli. The symbols next to the electrode names summarize the effects of direct electrical stimulation at each site.

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    Table 1.

    Details of the electrical brain stimulation procedure

    SiteAmplitude (mA)Duration (s)ADs?Unedited transcripts of the patient's and experimenters' dialogue
    DTIp4-342DTIp5-1Did you see anything there?
    22 sI don't know… I started feeling something… I don't know, it's probably just me…
    22NoAnything there?
    No.
    32DTIp4Anything here?
    8 sNo.
    DTIp2-122NoAnything here? Do you feel anything, see anything?
    Yeah, I feel like I… (looks perplexed, puts hand to forehead) I feel like I saw, like, some other site, we were at the train station…
    So it feels like you were in a subway?
    Yeah, outside the train station.
    22NoLet me know if you get any sensation like that again. Do you feel anything here? No?
    No, I… (doesn't continue)
    Did you see the train station, or did you feel like you were in the train station?
    I saw it.
    DTIp3-222NoLet me know if you feel or see anything here.
    Again, I saw almost like a… I don't know, like I saw… It was very brief…
    22NoI'm going to show it to you one more time. See if you can describe it any further.
    Um…
    24NoI'm going to give it to you one last time. What do you think?
    Um… I don't really know what to make out of it, but I saw like, another staircase… (pause) The rest I couldn't make out, but I saw a closet space, but not this (points to the closet facing him in the hospital room), that one was stuffed, and it was blue.
    Have you seen it before at some point in your life, you think?
    Yeah. I mean, when I saw the train station…
    The train station you'd been at.
    Yeah.
    22NoDid you see it again?
    Yeah, I saw it again.
    Same thing, staircase and…?
    Yeah.
    42DTIp3-1It is disturbing, or is it just weird?
    8 sIt's kind of weird.
    DTIp6-542NoLet me know if you see, feel or hear anything here.
    I felt something like a little, almost like if there was a rubber band (points to his own face, shows his cheeks).
    42NoI'm going to do it for you again.
    (looks surprised, puts hand to forehead) Your… face looked differently at that moment.
    The faces looked different? Did they twist on you?
    Yeah, your faces were all… slightly different.
    32No(patient is instructed to look straight at the experimenter's face) Let me know if it happens again.
    I… (doesn't continue)
    DTIp5-432DTIp4Let me know if the same sort of thing happens again.
    14 sIt did again.
    (during the afterdischarge) Is it still happening?
    Um, no. Only for that brief moment.
    What about the rest of my body?
    Yeah, I saw like… something else… (chuckles) I'm sorry… You all looked Italian… Like you were working in a pizza shop. That's what I saw, aprons and whatnot. Yeah, almost like you were working in a pizzeria. (chuckles)
    22NoLet me know if we're back in the pizzeria.
    (smiles, but says) No, not again.
    32DTIp4Let me know if you see it here again.
    6 s(chuckles) It was just a small change, but that's it, we went back.
    DTIp7-632NoLet me know if there is anything funny here.
    No.
    42NoHere?
    Nothing.
    DTIp8-742DTIp8-7Let me know if there's anything weird here.
    11 sNo.
    22DHb7Anything here?
    7 sNo.
    DHb6-522NoAnything there?
    A little bit of déjà vu.
    32DHb5-4I saw… Um, there was a strong déjà vu to it. It's a specific street around where I live. It's called (name of the street).
    4 sDid you see the street, or did it just feel like you were there?
    I saw it.
    DHb4-342DHb4-3Anything here?
    5 sYeah, I'm having that again. I saw that place and I felt the déjà vu… And I remember what I was thinking about. I think I was seeing… It was like my eye doctor's office or something like that. (later says it is an optometrist's office)
    DHb2-112NoLet me know if anything happens here.
    A little bit of déjà vu.
    22DHb2-1,(no further dialogue regarding this site)
    DHh2-1
    4 s
    • For each electrode pair, the stimulation amplitude and duration are tabulated, along with the location and duration of any afterdischarges (ADs) and the dialogue between the patient and the experimenters. The stimulation sites are presented in chronological order. Between stimulation of DTIp8-7 and DHb6-5, several other sites (not reported here) were stimulated (see Materials and Methods).

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The Journal of Neuroscience: 34 (16)
Journal of Neuroscience
Vol. 34, Issue 16
16 Apr 2014
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Seeing Scenes: Topographic Visual Hallucinations Evoked by Direct Electrical Stimulation of the Parahippocampal Place Area
Pierre Mégevand, David M. Groppe, Matthew S. Goldfinger, Sean T. Hwang, Peter B. Kingsley, Ido Davidesco, Ashesh D. Mehta
Journal of Neuroscience 16 April 2014, 34 (16) 5399-5405; DOI: 10.1523/JNEUROSCI.5202-13.2014

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Seeing Scenes: Topographic Visual Hallucinations Evoked by Direct Electrical Stimulation of the Parahippocampal Place Area
Pierre Mégevand, David M. Groppe, Matthew S. Goldfinger, Sean T. Hwang, Peter B. Kingsley, Ido Davidesco, Ashesh D. Mehta
Journal of Neuroscience 16 April 2014, 34 (16) 5399-5405; DOI: 10.1523/JNEUROSCI.5202-13.2014
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Keywords

  • direct electrical stimulation
  • functional magnetic resonance imaging
  • intracranial electroencephalography
  • parahippocampal place area
  • scene perception
  • visual hallucination

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