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Transcranial magnetic stimulation of the visual cortex in congenital blindness

Maurice Ptito1, 2* and Ron Kupers1, 2
  • 1 Université de Montreal, School of Optometry, Canada
  • 2 University of Copenhagen, Neuroscience and Pharmacology, Denmark

Introduction: For human and non-human primates, vision is one of the most privileged sensory channels used to interact with the environment. The importance of vision is strongly embedded in the organization of the brain as about one third of its cortical surface is involved in visual functions. It is therefore not surprising that the absence of vision from birth, or the loss of vision later in life, has huge consequences, both anatomically and functionally. We have shown in previous studies that, although, the visual system is largely atrophied by the loss of vision at birth, it is nonetheless present and can be activated by a variety of non-visual stimuli such as touch, audition and even smell. We present here a series of behavioral and brain imaging studies showing that the congenitally blind brain is capable of cross-modal plasticity and sensory substitution. Methods and results We recently showed that the occipital lobe of blind individuals is reduced in volume (whole brain Voxel Based Morphometry-VBM) (Ptito et al., 2008), has an increased cortical thickness (FreeSurfer and CIVET) and shows a supra-metabolic activity as revealed by fluoro-desoxy-glucose (18FDG-PET) (Kupers and Ptito, 2014) (Figure 1A, B, C respectively). Moreover, other non-visual structures in the blind brain were affected by early visual deprivation such as the posterior part of the right hippocampus (Chebat et al., 2007) and the splenium of the corpus callosum (Tomaiuolo et al., 2014), both regions showing a volumetric reduction. Figure 1. Structural and metabolic changes in the congenitally blind brain We used, in a series of experiments, a sensory substitution device coined the Tongue Display Unit or TDU. This apparatus translates an image grabbed by a camera into electrotactile pulses administered to the tongue via a grid of electrodes (Figure 2A). Figure 2. The tongue Display Unit (TDU) Congenitally blind (CB) subjects equipped with the TDU can learn to discriminate the orientation of a bar, discriminate motion and shapes (Ptito et al., 2009, 2012; Matteau et al., 2010). To do so, they activate regions of the brain that are visual in nature namely the visual cortex and the ventral and dorsal streams as revealed with functional Resonance Imaging (Figure 1B) (reviewed in Kupers and Ptito, 2014). Moreover the TDU has been successfully used as a navigation tool. CB individuals were able to point to, recognize and avoid obstacles while walking in a corridor (Chebat et al., 2011). Tested in an fMRI scanner in a virtual route recognition task, CB participants recruited not only their visual cortex but also the parahippocampal region, areas usually activated during topographical learning and spatial representation in sighted subjects (Kupers et al., 2010). To test for the functional role of visual cortical areas in blind, we used trans-cranial magnetic stimulation (TMS). Short repetitive TMS bursts applied over the mid-occipital cortex of the blind interfere with repetition priming effects of a list of words presented several times. Moreover, rTMS over the motion cortical area, which is part of the dorsal visual stream (area hMT+), induces an increase in the reaction times to moving stimuli in blind subjects only. We tested for the subjective experience associated with the activation of the visual cortex. While control seeing-subjects experienced visual phosphenes, blind participants reported parasthesiae (tingling sensations) either on the tongue or the fingers (figure 3). Finally, using somesthesic evoked potentials following learning with the TDU, we were able to show that the information originating in area SI was transferred to the primary visual cortex of the blind through increased cortico-cortical projections. Figure 3. TMS of the occipital cortex of blind subjects can induce tactile sensations referred to the tongue (A) and fingers (B). Conclusions The results obtained from this series of studies have valuable information on the nature of the plastic processes that take place in early blindness and might lead to the development of a new multisensory device that will use non-visual modalities to funnel sensory information to the visual cortex of the blind and help them “see”.

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Acknowledgements

The authors are indebted to these Foundations for their their generous support: The Harland Sanders Foundation (Canada), the Lundbeck Foundation (Denmark) and The Danish Medical Research Council FSS, Denmark).

References

1. Ptito M, Matteau I, Zhi Wang A, Paulson OB, Siebner HR, Kupers R. Crossmodal Recruitment of the ventral visual stream in congenital blindness. Neural Plast. 2012; 2012:304045.

2. Matteau I, Kupers R, Ricciardi E, Pietrini P, Ptito M. Beyond visual, aural and haptic movement perception: hMT+ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals. Brain Res Bull. 2010 82(5-6): 264-70.

3. Ptito M, Matteau I, Gjedde A, Kupers R. Recruitment of the middle temporal area by tactile motion in congenital blindness. Neuroreport. 2009 20(6): 543-7.

4. Kupers R, Ptito M. Compensatory plasticity and cross-modal reorganization following early visual deprivation. Neurosci Biobehav Rev. 2014 41:36-52.

5. Kupers R, Chebat DR, Madsen KH, Paulson OB, Ptito M. Neural correlates of virtual route recognition in congenital blindness. Proc Natl Acad Sci U S A. 1 2010 07:12716-21.

6. Chebat DR, Schneider FC, Kupers R, Ptito M. Navigation with a sensory substitution device in congenitally blind individuals. Neuroreport 2 2011 2:342-7.

7. Ptito M, Schneider FC, Paulson OB, Kupers R. Alterations of the visual pathways in congenital blindness. Exp Brain Res. 2008 187:41-9.

8. Tomaiuolo F, Campana S, Collins DL, Fonov VS, Ricciardi E, Sartori G, Pietrini P, Kupers R, Ptito M. Morphometric changes of the corpus callosum in congenital blindness. PLoS One 2014 9(9):e107871.

9. Chebat DR, Chen JK, Schneider F, Ptito A, Kupers R, Ptito M. Alterations in right posterior hippocampus in early blind individuals. Neuroreport 2007 18:329-33.

Keywords: Vision Disorders, Blindness, sensory substitution device (SSD), Neuroimaging (anatomic and functional), Transcranial magnetic stimulation (TMS)

Conference: International Conference - Educational Neuroscience, Abu Dhabi, United Arab Emirates, 28 Feb - 29 Feb, 2016.

Presentation Type: Oral Presentation (invited speakers only)

Topic: Educational Neuroscience

Citation: Ptito M and Kupers R (2016). Transcranial magnetic stimulation of the visual cortex in congenital blindness. Front. Neurosci. Conference Abstract: International Conference - Educational Neuroscience. doi: 10.3389/conf.fnins.2016.92.00013

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Received: 18 Jan 2016; Published Online: 23 Mar 2016.

* Correspondence: Prof. Maurice Ptito, Université de Montreal, School of Optometry, Montreal, Quebec, H3T 1P1, Canada, maurice.ptito@umontreal.ca