Cortical and subcortical proprioceptive contribution to oculomotor control in humans
Poster No:
2077
Submission Type:
Abstract Submission
Authors:
Daniela Balslev1, Graeme Keith2, Ross Hardaker2, Frances Crabe2, Alessio Fracasso2
Institutions:
1School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK, 2School of Psychology and Neuroscience, University of Glasgow, Glasgow, UK
First Author:
Co-Author(s):
Introduction:
Stretch receptors within the extraocular muscles convey information to the central nervous system about the rotation of the eyes. While precise control of limb position critically relies on proprioceptive feedback, a role for proprioception in controlling eye movements remains uncertain. To investigate whether the oculomotor network in the human brain respond to proprioceptive feedback, we acquired blood oxygen level dependent (BOLD) signal using ultra-high-field functional magnetic resonance imaging (7T fMRI), with a sequence optimized to focus on subcortical activation1. Previous studies conducted at lower magnetic field strength (3T) identified bilateral activity in the central sulcus (area 3A) and premotor cortex2. An unexpected finding was that the brainstem's extraocular motor nuclei that move the left eye responded to proprioceptive stimulation of the right eye's extraocular muscles3. We aimed to replicate those findings.
Methods:
Healthy adult volunteers (N=6) were asked to close their eyes and place their right index finger on the outer corner of their right eyelid. Following an auditory cue, they gently and briefly pushed the eyeball towards the nose, passively stretching the right lateral rectus muscle. Control conditions were designed to isolate motor and tactile task components. There were four conditions. Active: active eye movement; Passive: brief press (< 1 second) at the right corner of the right eye with their right index finger so that to gently move the eyeball. Touch: touch on the eyelid with their index finger, without moving the eyeball and Rest. Trials of each type were grouped in 25s blocks. Neural activity in response to eye proprioception was identified using the conjunction (Active – Rest) AND (Passive – Rest) masked exclusively with (Touch – Rest). The threshold for the conjunction was p<0.05 FDR-corrected for multiple comparisons, whereas for the exclusive mask it was more liberal (p<0.05, uncorrected). This contrast ruled out the confounding effects of finger movement or tactile stimulation on the eyelid. The task and the contrast were as described previously3.
All imaging was acquired using a 7T Magnetom Terra MRI scanner (Siemens, Erlangen, Germany) and single transmit, 32-channel receive radiofrequency head coil (Nova Medical Inc., Wilmington, MA, USA) with local ethical approval. Dielectric pads were used to improve the B1+ homogeneity4 with additional foam padding used to limit head movement. Functional data were acquired using a multi-band 2D echo-planar interleaved imaging (EPI) sequence5 with left to right phase-encoding and the following imaging parameters: 144 dynamics, resolution = 2 mm isotropic, 62 slices, field of view (FOV) = 192 x 192 x 124 mm, repetition time (TR) = 2500 ms, echo time (TE) = 17 ms1 , flip angle = 72°, multiband acceleration = 2. A short 2D-EPI scan (5 volumes) was acquired with the opposite phase encoding direction to correct for nonlinear geometric distortions.
After standard preprocessing (slice timing, realignment, distortion correction, normalisation to MNI space and smooting with FWHM= 2mm), data were analysed using a classic general linear model (3dDeconvolve in AFNI).
All imaging was acquired using a 7T Magnetom Terra MRI scanner (Siemens, Erlangen, Germany) and single transmit, 32-channel receive radiofrequency head coil (Nova Medical Inc., Wilmington, MA, USA) with local ethical approval. Dielectric pads were used to improve the B1+ homogeneity4 with additional foam padding used to limit head movement. Functional data were acquired using a multi-band 2D echo-planar interleaved imaging (EPI) sequence5 with left to right phase-encoding and the following imaging parameters: 144 dynamics, resolution = 2 mm isotropic, 62 slices, field of view (FOV) = 192 x 192 x 124 mm, repetition time (TR) = 2500 ms, echo time (TE) = 17 ms1 , flip angle = 72°, multiband acceleration = 2. A short 2D-EPI scan (5 volumes) was acquired with the opposite phase encoding direction to correct for nonlinear geometric distortions.
After standard preprocessing (slice timing, realignment, distortion correction, normalisation to MNI space and smooting with FWHM= 2mm), data were analysed using a classic general linear model (3dDeconvolve in AFNI).
Results:
The stretch of the right lateral rectus muscle was associated with suprathreshold activity not only in the somatosensory but also in the oculomotor network. In the brainstem we found a response to proprioceptive stimulation in the left abducens and left trigeminal nucleus which connect with the extraocular muscles of the left eye. This confirms previous findings at 3T3. We replicated the cortical activation identified previously2 and found additional foci in (oculo)motor structures like cerebellum and supplementary eye fields (Figure 1-2).
Conclusions:
This study confirms a proprioceptive coupling between the movement of the two eyes.
Motor Behavior:
Visuo-Motor Functions 1
Neuroanatomy, Physiology, Metabolism and Neurotransmission:
Subcortical Structures
Novel Imaging Acquisition Methods:
BOLD fMRI
Perception, Attention and Motor Behavior:
Perception: Tactile/Somatosensory 2
Keywords:
Brainstem
FUNCTIONAL MRI
HIGH FIELD MR
Motor
NORMAL HUMAN
Somatosensory
Sub-Cortical
Vision
1|2Indicates the priority used for review
·Figure 1. Subcortical activity in response to proprioceptive stimulation of the right lateral rectus muscle.Blue arrows: abducens nucleus; Purple arrows: spinal trigeminal nucleus.
·Figure 2. Cortical activity. Blue arrows: Supplementary Eye Field; Orange arrows: Central Sulcus(Area 3a)/Postcentral Gyrus (Area 2); Green arrows: Frontal Eye Field.
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2. Balslev, D., Albert, N. B. & Miall, C. Eye muscle proprioception is represented bilaterally in the sensorimotor cortex. Hum Brain Mapp 32, 624–631 (2011).
3. Balslev, D., Mitchell, A. G., Faria, P. J. M., Priba, L. & Macfarlane, J. A. Proprioceptive contribution to oculomotor control in humans. Hum Brain Mapp 43, 5081–5090 (2022).
4. Teeuwisse, W. M., Brink, W. M. & Webb, A. G. Quantitative assessment of the effects of high-permittivity pads in 7 Tesla MRI of the brain. Magn Reson Med 67, 1285–1293 (2012).
5. Moeller, S. et al. Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn Reson Med 63, 1144–1153 (2010).