Reduction of collinear inhibition in observers with central vision loss using anodal transcranial direct current stimulation: A case series
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Résumé
Current treatments for macular degenerative diseases can stabilize or slow disease progression but generally cannot provide a ‘cure’. As a result, a significant number of individuals with macular degeneration suffer from a loss of central vision that forces them to rely on para-central peripheral vision. Most patients with macular degeneration (84% of 1339 eyes) [[1]Fletcher D.C. Schuchard R.A. Preferred retinal loci relationship to macular scotomas in a low-vision population.Ophthalmology. 1997; 104: 632-638https://doi.org/10.1016/S0161-6420(97)30260-7Abstract Full Text PDF PubMed Scopus (254) Google Scholar] develop a preferred retinal locus (PRL): a specific para-central retinal region that is used for visual tasks in place of the fovea. However, the para-central retina is more susceptible to crowding (an inability to differentiate visual objects presented in ‘visual clutter’) [[2]Bouma H. Interaction effects in parafoveal letter recognition.Nature. 1970; 226: 177-178https://doi.org/10.1038/226177a0Crossref PubMed Scopus (884) Google Scholar]. This means that visual processing remains poor, even after spatial resolution limitations are addressed with appropriate magnification. Therefore, the reduction of crowding could be an effective rehabilitation strategy. Perceptual learning studies in individuals with normal vision [[3]Huang C.-B. Zhou J. Lu Z.-L. Feng L. Zhou Y. Binocular combination in anisometropic amblyopia.J Vis. 2009; 9 (17.1-1716)https://doi.org/10.1167/9.3.17Crossref Scopus (77) Google Scholar] and patients with central vision loss [[4]Maniglia M. Soler V. Cottereau B. Trotter Y. Spontaneous and training-induced cortical plasticity in MD patients: hints from lateral masking.Sci Rep. 2018; 8: 90https://doi.org/10.1038/s41598-017-18261-6Crossref PubMed Scopus (8) Google Scholar,[5]Chung S.T.L. Li R.W. Levi D.M. Crowding between first- and second-order letter stimuli in normal foveal and peripheral vision.J Vis. 2007; 7 (10.1-13)https://doi.org/10.1167/7.2.10Crossref Scopus (28) Google Scholar] have reported improvements in peripheral visual function with training. However, perceptual learning requires extensive training and gains are typically specific to the trained stimulus. Nevertheless, these findings indicate that the neural mechanisms contributing to crowding in peripheral vision are plastic. Non-invasive brain stimulation techniques such as anodal direct current stimulation (a-tDCS) offer an alternative approach to improving peripheral visual function [[6]Reinhart R.M.G. Xiao W. McClenahan L.J. Woodman G.F. Electrical stimulation of visual cortex can immediately improve spatial vision.Curr Biol. 2016; 26: 1867-1872https://doi.org/10.1016/j.cub.2016.05.019Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar,[7]Bonder T. Gopher D. Yeshurun Y. The joint effects of spatial cueing and transcranial direct current stimulation on visual acuity.Front Psychol. 2018; 9: 159https://doi.org/10.3389/fpsyg.2018.00159Crossref PubMed Scopus (7) Google Scholar]. Using a-tDCS over the visual cortex, we have recently demonstrated that collinear inhibition can be reduced in observers with normal vision [[8]Raveendran R.N. Tsang K. Tiwana D. Chow A. Thompson B. Anodal transcranial direct current stimulation reduces collinear lateral inhibition in normal peripheral vision.PloS One. 2020; 15e0232276https://doi.org/10.1371/journal.pone.0232276Crossref PubMed Scopus (5) Google Scholar]. Collinear inhibition refers to the impaired detectability of a visual target when it is flanked by similarly oriented high contrast targets and is one of the low-level mechanisms involved in visual crowding [[9]Lev M. Polat U. Space and time in masking and crowding.J Vis. 2015; 15: 10https://doi.org/10.1167/15.13.10Crossref PubMed Scopus (27) Google Scholar]. Building on this previous work, in this case series of three patients with central vision loss, we tested whether a-tDCS could be used to modulate the neural mechanisms that contribute to crowding in a clinical population. 5 participants (4 females; age: 55 ± 22 years) diagnosed with macular degeneration agreed to participate in this study. Participants were excluded if they had multiple PRLs and any contraindications to transcranial electrical stimulation. Two participants were excluded due to a history of epilepsy and a preexisting heart condition. Data for the remaining three participants were collected at the School of Optometry and Vision Science, University of Waterloo, Waterloo, Canada (n = 2) and the Envision Research Institute, Wichita, USA (n = 1). All participants provided written, informed consent. The study was approved by the University of Waterloo and Wichita State University research ethics committees. All the procedures involved in this research adhered to the tenets of the Declaration of Helsinki. A sham controlled, single-blind study design was used to test the effect of visual cortex a-tDCS on collinear inhibition. Patients with macular degeneration performed a 2AFC contrast detection task with collinear flankers positioned at a distance of 3λ from the target (collinear inhibition) or 6λ (collinear facilitation). Participants were encouraged to adopt their habitual head position so that they could see the fixation cross clearly and fixation was monitored using an infrared video-based eyetracker. Each patient completed two randomized sessions: real anodal-tDCS or sham tDCS. tDCS was administered using a commercially available DC Stimulator (NeuroConn MC). The electrical current was administered using two 5 cm × 5 cm rubber electrodes placed inside saline soaked sponges. The electrodes were secured using a head strap and placed over Oz (anodal electrode) and Cz (cathodal electrode) based on the 10–20 EEG electrode positioning system. Active stimulation involved 2 mA of anodal tDCS for 20 minutes. Sham stimulation involved a 5 second ramp up of current immediately followed by a 5 second ramp down with the electrodes left in place for 20 minutes. Active and sham stimulation visits took place on two different days and each visit was separated by at least 48 hours. The order of stimulation was also randomized. During each visit, all participants completed 4 sessions of contrast threshold measurements: pre-, during-, 5min post- and 30min post-stimulation (Supplementary Figure 1). All participants completed the two study sessions without reporting any adverse effects. However, participant S3 could not complete the 6λ viewing condition. Fig. 1 shows the mean normalized contrast thresholds for the collinear inhibition condition for the active and sham stimulation sessions. The mean contrast threshold values and staircase reversal standard deviations for every participant for the collinear inhibition and facilitation viewing conditions are provided in Supplementary Table 1. A reduction of collinear inhibition is apparent for the active but not the sham stimulation conditions for all participants. With a single session of a-tDCS, an average 56% (38%–76%) reduction of collinear inhibition was sustained after 30min of stimulation. Our preliminary case series results indicate that it may be possible to alleviate lateral inhibition and perhaps other components of crowding in patients with macular degeneration by directly altering cortical processing with non-invasive brain stimulation. These observations provide a foundation for larger studies into the use of visual cortex a-tDCS to improve visual function in patients with central vision loss. Recent technological advances have enabled tDCS to be delivered as a home based therapy (for instance, https://soterixmedical.com/research/remote) meaning that such studies can be more easily accomplished. The authors confirm there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that influenced its outcome. This research was funded by the LCI Foundation (RNR), CFI grant 34095(BT) and NSERC grants RPIN-05394 and RGPAS-477166 (BT). The following is the Supplementary data to this article: Download .docx (.17 MB) Help with docx files Multimedia component 1 We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us. We further confirm that any aspect of the work covered in this manuscript that has involved either experimental animals or human patients has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the manuscript. We understand that the Corresponding Author is the sole contact for the Editorial process (including Editorial Manager and direct communications with the office). He/she is responsible for communicating with the other authors about progress, submissions of revisions and final approval of proofs. We confirm that we have provided a current, correct email address which is accessible by the Corresponding Author and which has been configured to accept email from [email protected] . Repetitive measurements prolong the after-effects of transcranial direct current stimulation (tDCS) on crowdingBrain Stimulation: Basic, Translational, and Clinical Research in NeuromodulationPreviewThis article has been withdrawn at the request of the author(s) and/or editor. The Publisher apologizes for any inconvenience this may cause. The full Elsevier Policy on Article Withdrawal can be found at https://www.elsevier.com/about/our-business/policies/article-withdrawal . Full-Text PDF Open AccessWithdrawn: Reply to letter to the editorBrain Stimulation: Basic, Translational, and Clinical Research in NeuromodulationPreviewThis article has been withdrawn at the request of the author(s) and/or editor. The Publisher apologizes for any inconvenience this may cause. The full Elsevier Policy on Article Withdrawal can be found at https://www.elsevier.com/about/our-business/policies/article-withdrawal . Full-Text PDF Open Access
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La notice
- Revue
- Brain stimulation
- Thématique
- Visual perception and processing mechanisms
- Domaine
- Neuroscience
- Établissements canadiens
- University of Waterloo
- Organismes subventionnaires
- —
- Mots-clés
- Macular degenerationPeripheral visionOphthalmologyMedicineOptometryRetinalPopulationPsychologyArtificial intelligenceComputer science
- Résumé présent dans OpenAlex
- oui