Periodic Report Summary - EYE POSITION (How do cortical representations of eye position impact spatial cognition?)
Without an accurate cortical representation of the eye rotation in the orbit it would be impossible to reach to visual targets or to match a person and a voice in a crowd based on their common location. The projection of visual objects on the retina changes with the movement of the eyes, so eye position information is necessary to anchor visual objects to sounds or hand locations by transforming retinal into head- and body-centred coordinates. Eye position thus aligns the visual space with the space of other sensory modalities and the motor space and is therefore likely to contribute to building abstract, multimodal, representations of space necessary for instance to direct exploratory eye movements or to orient attention.
The project aimed to characterise the role of eye muscle proprioception in visual localisation, attention and space exploration.
(1) The role of eye proprioception in visual localisation
There are two main signals that convey eye position to the brain: the efference copy of the oculomotor command or the corollary discharge and the afferent input from the eye muscles or proprioception. Despite a century-long debate about the efference copy versus sensory re-afference the question whether visual localisation relies on corollary discharge (von Helmholtz, 1925) or eye proprioception (Sherrington, 1918) is still unanswered and experimental observations seem contradictory. By investigating a patient with a focal lesion in the somatosensory cortex, I was able to show that eye proprioception is used only when it mismatches the oculomotor command. In normal conditions, the brain prefers the fast corollary discharge, while monitoring eye proprioception continuously, ready to use it as soon as a mismatch is detected. This conclusion opens new lines of research to understand how the brain compares and updates the eye position signals to accurately locate visual objects despite changes in the eye muscles, for instance during growth or after surgery.
- D. Balslev, M. Himmelbach, H.-O. Karnath, S. Borchers, B. Odoj. (2012) Eye proprioception used for visual localisation only if in conflict with the oculomotor plan. J Neuroscience 32:8569-73 (See http://www.ncbi.nlm.nih.gov/pubmed/22723697(opens in new window) online for further details.)
(2) The role of eye proprioception in spatial attention
My experiments in healthy humans showed that a lasting decrease of activity in the somatosensory cortex induced with repetitive transcranial magnetic stimulation (TMS) alters the perception of one's own eye position and reduces the ability to correct for a proprioceptive perturbation (Balslev and Miall, J Neurosci, 2008). An observation while using this method has been that decreasing the excitability of the somatosensory cortex also changes stimulus visibility (Balslev, Gowen and Miall, J Cogn Neurosci, 2011). This observation is very intriguing because the somatosensory cortex is not part of the cortical attention network, which consists of the intraparietal sulcus, frontal eye field and temporo-parietal junction. To investigate whether this effect is caused by eye proprioception, as opposed to for instance a spread of induced current to adjacent posterior parietal cortex, I used a sclera lens to induce a sustained rotation of the non-viewing, dominant eye, stimulating the extraocular muscle proprioceptors. While participants viewed a display with the non-dominant eye, this procedure improved visual detection in the hemifield located in the direction of this rotation. This suggests that eye proprioception plays a role in the allocation of attention in the visual space.
- D. Balslev, W. Newman, P.C. Knox (2012) Extraocular muscle afferent signals modulate visual attention. Investigative Ophthalmology & Visual Science (in press) (See http://www.ncbi.nlm.nih.gov/pubmed/22977139(opens in new window) online for further details.)
A combined TMS and functional magnetic resonance imaging (fMRI) experiment revealed that this role is presumably mediated by a modulatory connection from the somatosensory to the higher-order visual cortex
- D. Balslev, H. R. Siebner, O.B. Paulson, T. Kassuba (2012) The cortical eye proprioceptive signal modulates neural activity in higher-order visual cortex as predicted by the variation in visual sensitivity. Neuroimage 61: 950-956 (See http://dx.doi.org/10.1016/j.neuroimage.2012.04.007(opens in new window) online for further details.)
(3) The role of eye proprioception in spatial exploration
To investigate the role of eye proprioception in spatial exploration we took advantage of the rare opportunity to test a patient with a focal lesion confined to the right postcentral gyrus. In this patient we found a bias in visual search and in visual sensitivity towards the centre of the orbit (e.g. towards the left visual hemifield in rightward gaze). Given this direction-specific effect of an isolated postcentral lesion on visuospatial attention, in a second study we asked whether co-injury of the somatosensory cortex and the right perisylvian network - the latter is typically associated with spatial neglect and a spontaneous rightward eye deviation - might reduce the rightward orienting bias in neglect. A voxel-wise lesion behavior mapping (VLBM) analysis of a group of 15 stroke patients with neglect-typical right perisylvian lesions confirmed this hypothesis. Taken together the results suggest that somatosensory cortex is part of a neural circuit controlling the prioritisation of visual space.
- Balslev, Odoj and Karnath. A role of somatosensory cortex in spatial attention (submitted) Odoj and Balslev. Visual sensitivity shifts with perceived eye position (submitted).
Conclusion
Whereas the role of eye proprioception in visual localisation appears to be minor, this project has revealed a reliable and intriguing effect of this sensory modality in visuospatial attention in both healthy and in spatial neglect populations. This opens further avenues for research aimed at understanding the mechanisms of these effects, the interaction of this area with the cortical and subcortical attention networks and the role of somatosensory cortex in spatial neglect.
Project website: http://www.danielabalslev.dk/research/(opens in new window)
The project aimed to characterise the role of eye muscle proprioception in visual localisation, attention and space exploration.
(1) The role of eye proprioception in visual localisation
There are two main signals that convey eye position to the brain: the efference copy of the oculomotor command or the corollary discharge and the afferent input from the eye muscles or proprioception. Despite a century-long debate about the efference copy versus sensory re-afference the question whether visual localisation relies on corollary discharge (von Helmholtz, 1925) or eye proprioception (Sherrington, 1918) is still unanswered and experimental observations seem contradictory. By investigating a patient with a focal lesion in the somatosensory cortex, I was able to show that eye proprioception is used only when it mismatches the oculomotor command. In normal conditions, the brain prefers the fast corollary discharge, while monitoring eye proprioception continuously, ready to use it as soon as a mismatch is detected. This conclusion opens new lines of research to understand how the brain compares and updates the eye position signals to accurately locate visual objects despite changes in the eye muscles, for instance during growth or after surgery.
- D. Balslev, M. Himmelbach, H.-O. Karnath, S. Borchers, B. Odoj. (2012) Eye proprioception used for visual localisation only if in conflict with the oculomotor plan. J Neuroscience 32:8569-73 (See http://www.ncbi.nlm.nih.gov/pubmed/22723697(opens in new window) online for further details.)
(2) The role of eye proprioception in spatial attention
My experiments in healthy humans showed that a lasting decrease of activity in the somatosensory cortex induced with repetitive transcranial magnetic stimulation (TMS) alters the perception of one's own eye position and reduces the ability to correct for a proprioceptive perturbation (Balslev and Miall, J Neurosci, 2008). An observation while using this method has been that decreasing the excitability of the somatosensory cortex also changes stimulus visibility (Balslev, Gowen and Miall, J Cogn Neurosci, 2011). This observation is very intriguing because the somatosensory cortex is not part of the cortical attention network, which consists of the intraparietal sulcus, frontal eye field and temporo-parietal junction. To investigate whether this effect is caused by eye proprioception, as opposed to for instance a spread of induced current to adjacent posterior parietal cortex, I used a sclera lens to induce a sustained rotation of the non-viewing, dominant eye, stimulating the extraocular muscle proprioceptors. While participants viewed a display with the non-dominant eye, this procedure improved visual detection in the hemifield located in the direction of this rotation. This suggests that eye proprioception plays a role in the allocation of attention in the visual space.
- D. Balslev, W. Newman, P.C. Knox (2012) Extraocular muscle afferent signals modulate visual attention. Investigative Ophthalmology & Visual Science (in press) (See http://www.ncbi.nlm.nih.gov/pubmed/22977139(opens in new window) online for further details.)
A combined TMS and functional magnetic resonance imaging (fMRI) experiment revealed that this role is presumably mediated by a modulatory connection from the somatosensory to the higher-order visual cortex
- D. Balslev, H. R. Siebner, O.B. Paulson, T. Kassuba (2012) The cortical eye proprioceptive signal modulates neural activity in higher-order visual cortex as predicted by the variation in visual sensitivity. Neuroimage 61: 950-956 (See http://dx.doi.org/10.1016/j.neuroimage.2012.04.007(opens in new window) online for further details.)
(3) The role of eye proprioception in spatial exploration
To investigate the role of eye proprioception in spatial exploration we took advantage of the rare opportunity to test a patient with a focal lesion confined to the right postcentral gyrus. In this patient we found a bias in visual search and in visual sensitivity towards the centre of the orbit (e.g. towards the left visual hemifield in rightward gaze). Given this direction-specific effect of an isolated postcentral lesion on visuospatial attention, in a second study we asked whether co-injury of the somatosensory cortex and the right perisylvian network - the latter is typically associated with spatial neglect and a spontaneous rightward eye deviation - might reduce the rightward orienting bias in neglect. A voxel-wise lesion behavior mapping (VLBM) analysis of a group of 15 stroke patients with neglect-typical right perisylvian lesions confirmed this hypothesis. Taken together the results suggest that somatosensory cortex is part of a neural circuit controlling the prioritisation of visual space.
- Balslev, Odoj and Karnath. A role of somatosensory cortex in spatial attention (submitted) Odoj and Balslev. Visual sensitivity shifts with perceived eye position (submitted).
Conclusion
Whereas the role of eye proprioception in visual localisation appears to be minor, this project has revealed a reliable and intriguing effect of this sensory modality in visuospatial attention in both healthy and in spatial neglect populations. This opens further avenues for research aimed at understanding the mechanisms of these effects, the interaction of this area with the cortical and subcortical attention networks and the role of somatosensory cortex in spatial neglect.
Project website: http://www.danielabalslev.dk/research/(opens in new window)