Lying in a 3T MRI scanner induces neglect-like spatial attention bias

  1. Axel Lindner
  2. Daniel Wiesen
  3. Hans-Otto Karnath

  • Curated by eLife

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    Evaluation Summary:

    This paper examines the visual-ocular response in participants when exposed to the static magnetic field of a 3T MRI system. Historically, this problem has been approached from a safety perspective. In the present study, the authors ask about the behavioral consequences of this field given that it induces a response in the vestibular system, hypothesized to mimic that of a caloric vestibular stimulation event. As such, one should anticipate a biased vestibulo-ocular reflex in the static field as well as biases in spatial attention. These predictions were confirmed, with the attentional bias manifest in eye movements during a visual search task. This is an important finding because it reveals functional "artifacts" that may arise during fMRI studies, effects that may need to be considered by those conducting research in the MR environment (especially functional studies).

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)

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Abstract

The static magnetic field of MRI scanners can induce a magneto-hydrodynamic stimulation of the vestibular organ (MVS). In common fMRI settings, this MVS effect leads to a vestibular ocular reflex (VOR). We asked whether – beyond inducing a VOR – putting a healthy subject in a 3T MRI scanner would also alter goal-directed spatial behavior, as is known from other types of vestibular stimulation. We investigated 17 healthy volunteers, all of which exhibited a rightward VOR inside the MRI-scanner as compared to outside-MRI conditions. More importantly, when probing the distribution of overt spatial attention inside the MRI using a visual search task, subjects scanned a region of space that was significantly shifted toward the right. An additional estimate of subjective straight-ahead orientation likewise exhibited a rightward shift. Hence, putting subjects in a 3T MRI-scanner elicits MVS-induced horizontal biases of spatial orienting and exploration, which closely mimic that of stroke patients with spatial neglect.

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  1. Version published to 10.7554/elife.71076 on eLife
  2. eLife

    Evaluation Summary:

    This paper examines the visual-ocular response in participants when exposed to the static magnetic field of a 3T MRI system. Historically, this problem has been approached from a safety perspective. In the present study, the authors ask about the behavioral consequences of this field given that it induces a response in the vestibular system, hypothesized to mimic that of a caloric vestibular stimulation event. As such, one should anticipate a biased vestibulo-ocular reflex in the static field as well as biases in spatial attention. These predictions were confirmed, with the attentional bias manifest in eye movements during a visual search task. This is an important finding because it reveals functional "artifacts" that may arise during fMRI studies, effects that may need to be considered by those conducting research in the MR environment (especially functional studies).

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    The authors have studied the visual-ocular response in subjects who were exposed to a static magnetic field of 3 tesla. This magnetic field strength is only encountered in the environment of a high field magnetic resonance scanner. The magnetic field induces a response in the vestibular system, and which is highly dependent on head orientation with respect to the magnetic field. The response is hypothesised to mimic that of a caloric vestibular stimulation event. The authors have constructed a very well-designed study to determine the bias in fully dark conditions following a specific visual cued tracking point. The eye movements were tracked with an infra-red camera to ensure completely dark conditions. Data is presented and statistical analysis given which supports the author's questions and hypothesis.

    In a historical context this article is a further development of the field of interest in the effect of magnetic fields on the human senses. Originally the questions were ones of bio-mechanism involved and safety of MRI. Now those questions are largely satisfied, the field moves to using the observed effects for neuroscience and even clinical applications (in their broadest terms). The authors show a distinct bias in visual tracking which could potentially be used as a model for stroke patients with spatial neglect. There are also implications for those studying default networks or visual tracking using fMRI. The effect measured here is still quite subtle at 3 T, but has implications for higher field fMRI at 7 T or even higher.

  4. eLife

    Reviewer #2 (Public Review):

    Overall, the study is well written, appropriately analyzed, and the methods are clear and well described. I appreciate the simple and straightforward differential in the study design, the authors attempt to maximize the stimulus within the confines of the head coil, and the presentation of the data. The magnetic field used here (3 Tesla) is commonly used in research and increasingly used in clinical MRI scans. The only major comment is that the relationship between the VOR and visual tasks was not analyzed-which seems to me to be a key relationship. A process of adaptation occurs in the MRI machine that is reflected in the after effect where nystagmus (and sense of rotation) reverses direction if the participant spends greater than a few minutes in the MRI. These effects occur on a time scale that would be lost by averaging over a 10 minute period. Nevertheless, the authors achieved their objective of determining whether there is a spatial bias induced by the MRI magnetic field. The temporal effects would not detract from the principle discovery that the MRI machine induces a spatial bias. The results will have implications for fMRI studies and may lead to new ways of treating spatial neglect.

    Studies have also found that the perception of vertigo is shorter than the nystagmus time-constant. What is the strength of the relationship between VOR slow-phase eye velocity and saccade bias? As commented on in the supplement material, typical MVS VOR shows adaptation within a minute or two. Does the VOR and saccade bias follow a similar time-constant?

  5. eLife

    Reviewer #3 (Public Review):

    The authors report a study in which they show that the involuntary eye movements induced by immersion within the dense magnetic field of an MRI scanner lateralises the spatial deployment of visual attention. This is an important finding because it shows, for the first time, that this source of involuntary movement is of functional significance. The implication is that an individual who is placed within a scanner will likely show attentional biases and vestibular-based neural activations that may need to be accommodated by relevant control conditions/participant groups. In short, the very procedure of imaging the metabolic processes that underpin visual cognition has now been shown to induce visual artifacts that need separate consideration. More generally, the study reaffirms the pervasive effect of vestibular stimulation on lateralised visuo-spatial behaviour.

    The experimental methodology appears robust, and the data interpretation raises no real concern.

    My main query is the extent to which the findings are generalisable. The visual search task (and straight ahead task) were conducted in complete darkness which is, of course, an uncommon viewing condition. One would expect the degree of bias to be strongest under such conditions, and the question arises as to how much the bias is weakened when other stimuli, especially those in the 'neglected' field or which are strongly salient, become visible and compete for attention? On a related note, the degree of bias may also be weakened in scanners that generate a smaller (e.g. 1.5T) magnetic field.

    My other query concerns the author's suggestion that MRI exposure could be used to help treat unilateral perceptual disorders such as hemi-spatial neglect. One questions the effectiveness of this approach given (1) the cost and availability of MRI, not least relative to the galvanic and caloric vestibular stimulators that are available and which enable a more diverse range of stimulation protocols, and (2) the patient burden associated with having to lie inside a high-strength scanner, likely exacerbated in the case of neglect by the presence of allied motor impairment and/or contraindicated by the presence of metal inside the body.

  6. Version published to 10.1101/2021.06.07.447306v1 on bioRxiv