Hearing colors: an example of brain plasticity

Arantxa Alfaro, Ángela Bernabeu, Carlos Agulló, Jaime Parra, Eduardo Fernández, Arantxa Alfaro, Ángela Bernabeu, Carlos Agulló, Jaime Parra, Eduardo Fernández

Abstract

Sensory substitution devices (SSDs) are providing new ways for improving or replacing sensory abilities that have been lost due to disease or injury, and at the same time offer unprecedented opportunities to address how the nervous system could lead to an augmentation of its capacities. In this work we have evaluated a color-blind subject using a new visual-to-auditory SSD device called "Eyeborg", that allows colors to be perceived as sounds. We used a combination of neuroimaging techniques including Functional Magnetic Resonance Imaging (fMRI), Diffusion Tensor Imaging (DTI) and proton Magnetic Resonance Spectroscopy ((1)H-MRS) to study potential brain plasticity in this subject. Our results suggest that after 8 years of continuous use of this device there could be significant adaptive and compensatory changes within the brain. In particular, we found changes in functional neural patterns, structural connectivity and cortical topography at the visual and auditive cortex of the Eyeborg user in comparison with a control population. Although at the moment we cannot claim that the continuous use of the Eyeborg is the only reason for these findings, our results may shed further light on potential brain changes associated with the use of other SSDs. This could help to better understand how the brain adapts to several pathologies and uncover adaptive resources such as cross-modal representations. We expect that the precise understanding of these changes will have clear implications for rehabilitative training, device development and for more efficient programs for people with disabilities.

Keywords: blindness; diffusion tensor imaging (DTI); functional magnetic resonance imaging (fMRI); magnetic resonance spectroscopy; neuroplasticity; sensory substitution device (SSD); visual cortex.

Figures

Figure 1
Figure 1
Visual stimulus and Functional Magnetic Resonance Imaging (fMRI) activation in the Eyeborg user and the control group. (A) Protocol of the Farnsworth-Munsell test. Within each scan series, the stimulus alternated between blocks of chromatic or achromatic discrimination trials and fixation. (B) Areas showing a significant response to chromatic stimulation in the Eyeborg user. (C) Areas showing a significant response to chromatic stimulation in two representative controls (single subjects). (D) Statistical parametric maps of the Eyeborg user are shown in standard anatomical space. (E) Statistical parametric maps of the whole control population in standard anatomical space.
Figure 2
Figure 2
Analysis of the paradigm involving the presentation of simultaneously visual and auditory stimulation. (A) Data corresponding to the Eyeborg user (single subject analysis) showing a strong effect on temporal and occipital cortex. (B) Averaged activation of the control group in response to the same paradigm of stimulation.
Figure 3
Figure 3
Tractography results. (A) Callosal fiber tracks in the Eyeborg user. (B) Callosal fiber tracks in a representative control subject (matched in age and sex). (C) Left inferior fronto-occipital fasciculus (IFOF), which connects the ventral occipital lobe and the orbitofrontal cortex, in the Eyeborg user. (D) Enlargement of the IFOF displayed in panel (C). The arrow points the region with increased myelin density related to the temporal lobe.

References

    1. Abboud S., Hanassy S., Levy-Tzedek S., Maidenbaum S., Amedi A. (2014). EyeMusic: introducing a “visual” colorful experience for the blind using auditory sensory substitution. Restor. Neurol Neurosci. 32, 247–257. 10.3233/RNN-130338
    1. Amedi A., Stern W. M., Camprodon J. A., Bermpohl F., Merabet L., Rotman S., et al. . (2007). Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat. Neurosci. 10, 687–689. 10.1038/nn1912
    1. Bavelier D., Levi D. M., Li R. W., Dan Y., Hensch T. K. (2010). Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964–14971. 10.1523/JNEUROSCI.4812-10.2010
    1. Beauchamp M. S., Haxby J. V., Jennings J. E., DeYoe E. A. (1999). An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. Cereb. Cortex 9, 257–263. 10.1093/cercor/9.3.257
    1. Bernabeu A., Alfaro A., García M., Fernández E. (2009). Proton magnetic resonance spectroscopy (1H-MRS) reveals the presence of elevated myo-inositol in the occipital cortex of blind subjects. Neuroimage 47, 1172–1176. 10.1016/j.neuroimage.2009.04.080
    1. Bologna G., Deville B., Pun T. (2009). On the use of the auditory pathway to represent image scenes in real-time. Neurocomputing 72, 839–849 10.1016/j.neucom.2008.06.020
    1. Capelle C., Trullemans C., Arno P., Veraart C. (1998). A real-time experimental prototype for enhancement of vision rehabilitation using auditory substitution. IEEE Trans. Biomed. Eng. 45, 1279–1293. 10.1109/10.720206
    1. Catani M., Jones D. K., Donato R., Ffytche D. H. (2003). Occipito-temporal connections in the human brain. Brain 126, 2093–2107. 10.1093/brain/awg203
    1. Catani M., Mesulam M. (2008). The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex 44, 953–961. 10.1016/j.cortex.2008.04.002
    1. Catani M., Thiebaut de Schotten M. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44, 1105–1132. 10.1016/j.cortex.2008.05.004
    1. Cohen L. G., Celnik P., Pascual-Leone A., Corwell B., Falz L., Dambrosia J., et al. . (1997). Functional relevance of cross-modal plasticity in blind humans. Nature 389, 180–183. 10.1038/38278
    1. Connell N., Merabet L. B. (2014). Uncovering the connectivity of the brain in relation to novel vision rehabilitation strategies. Neurology 83, 484–485. 10.1212/WNL.0000000000000664
    1. Cramer S. C., Sur M., Dobkin B. H., O’Brien C., Sanger T. D., Trojanowski J. Q., et al. . (2011). Harnessing neuroplasticity for clinical applications. Brain 134, 1591–1609. 10.1093/brain/awr039
    1. Cronly-Dillon J., Persaud K., Gregory R. P. (1999). The perception of visual images encoded in musical form: a study in cross-modality information transfer. Proc. Biol. Sci. 266, 2427–2433. 10.1098/rspb.1999.0942
    1. Engel S. A., Rumelhart D. E., Wandell B. A., Lee A. T., Glover G. H., Chichilnisky E. J., et al. . (1994). fMRI of human visual cortex. Nature 369:525. 10.1038/369525a0
    1. Eyeborg (2015). Available online at: . Accessed on 2015.
    1. Fabri M., Pierpaoli C., Barbaresi P., Polonara G. (2014). Functional topography of the corpus callosum investigated by DTI and fMRI. World J. Radiol. 6, 895–906. 10.4329/wjr.v6.i12.895
    1. Fernandez E., Merabet L. B. (2011). “Cortical plasticity and reorganization in severe vision loss,” in Visual Prosthetics, ed Dagnelie G. (New York, NY: Springer; ), 77–92.
    1. Fernández E., Pelayo F., Romero S., Bongard M., Marin C., Alfaro A., et al. . (2005). Development of a cortical visual neuroprosthesis for the blind: the relevance of neuroplasticity. J. Neural Eng. 2, R1–R12. 10.1088/1741-2560/2/4/r01
    1. Goebel R., Esposito F., Formisano E. (2006). Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum. Brain Mapp. 27, 392–401. 10.1002/hbm.20249
    1. Haga K. K., Khor Y. P., Farrall A., Wardlaw J. M. (2009). A systematic review of brain metabolite changes, measured with 1H magnetic resonance spectroscopy, in healthy aging. Neurobiol. Aging 30, 353–363. 10.1016/j.neurobiolaging.2007.07.005
    1. Hensch T. K., Fagiolini M. (2005). Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 147, 115–124. 10.1016/s0079-6123(04)47009-5
    1. Kahol K., French J., Bratton L., Panchanathan S. (2006). Learning and perceiving colors haptically. Proc. ASSETS 173–180 10.1145/1168987.1169017
    1. Kantarci K. (2014). Fractional anisotropy of the fornix and hippocampal atrophy in Alzheimer’s disease. Front. Aging Neurosci. 6:316. 10.3389/fnagi.2014.00316
    1. Kellenbach M. L., Hovius M., Patterson K. (2005). A pet study of visual and semantic knowledge about objects. Cortex 41, 121–132. 10.1016/s0010-9452(08)70887-6
    1. Kikuta K., Takagi Y., Nozaki K., Hanakawa T., Okada T., Miki Y., et al. . (2006). Early experience with 3-T magnetic resonance tractography in the surgery of cerebral arteriovenous malformations in and around the visual pathway. Neurosurgery 58, 331–337; discussion 331–337. 10.1227/01.neu.0000195017.82776.90
    1. Maidenbaum S., Abboud S., Amedi A. (2014). Sensory substitution: closing the gap between basic research and widespread practical visual rehabilitation. Neurosci. Biobehav. Rev. 41, 3–15. 10.1016/j.neubiorev.2013.11.007
    1. Meijer P. B. (1992). An experimental system for auditory image representations. IEEE Trans. Biomed. Eng. 39, 112–121. 10.1109/10.121642
    1. Merabet L. B., Pascual-Leone A. (2010). Neural reorganization following sensory loss: the opportunity of change. Nat. Rev. Neurosci. 11, 44–52. 10.1038/nrn2758
    1. Naressi A., Couturier C., Castang I., de Beer R., Graveron-Demilly D. (2001). Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput. Biol. Med. 31, 269–286. 10.1016/s0010-4825(01)00006-3
    1. Nie M., Ren J., Li Z., Niu J., Qiu Y., Zhu Y., et al. . (2009). SoundView: an auditory guidance system based on environment understanding for the visually impaired people. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 7240–7243. 10.1109/IEMBS.2009.5334754
    1. Nilsson C., Markenroth Bloch K., Brockstedt S., Lätt J., Widner H., Larsson E. M. (2007). Tracking the neurodegeneration of parkinsonian disorders–a pilot study. Neuroradiology 49, 111–119. 10.1007/s00234-006-0165-1
    1. Nudo R. J. (2006). Plasticity. NeuroRx 3, 420–427. 10.1016/j.nurx.2006.07.006
    1. Pascual-Leone A., Amedi A., Fregni F., Merabet L. B. (2005). The plastic human brain cortex. Annu. Rev. Neurosci. 28, 377–401. 10.1146/annurev.neuro.27.070203.144216
    1. Poirier C., De Volder A., Tranduy D., Scheiber C. (2007). Pattern recognition using a device substituting audition for vision in blindfolded sighted subjects. Neuropsychologia 45, 1108–1121. 10.1016/j.neuropsychologia.2006.09.018
    1. Poveda M. J., Bernabeu A., Concepción L., Roa E., de Madaria E., Zapater P., et al. . (2010). Brain edema dynamics in patients with overt hepatic encephalopathy a magnetic resonance imaging study. Neuroimage 52, 481–487. 10.1016/j.neuroimage.2010.04.260
    1. Proulx M. J., Ptito M., Amedi A. (2014). Multisensory integration, sensory substitution and visual rehabilitation. Neurosci. Biobehav. Rev. 41, 1–2. 10.1016/j.neubiorev.2014.03.004
    1. Ptito M., Moesgaard S. M., Gjedde A., Kupers R. (2005). Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. Brain 128, 606–614. 10.1093/brain/awh380
    1. Striem-Amit E., Guendelman M., Amedi A. (2012). ‘Visual’ acuity of the congenitally blind using visual-to-auditory sensory substitution. PLoS One 7:e33136. 10.1371/journal.pone.0033136
    1. Tregellas J. R., Ellis J., Shatti S., Du Y. P., Rojas D. C. (2009). Increased hippocampal, thalamic and prefrontal hemodynamic response to an urban noise stimulus in schizophrenia. Am. J. Psychiatry 166, 354–360. 10.1176/appi.ajp.2008.08030411
    1. Wakana S., Jiang H., Nagae-Poetscher L. M., van Zijl P. C., Mori S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology 230, 77–87. 10.1148/radiol.2301021640
    1. Weaver K. E., Richards T. L., Saenz M., Petropoulos H., Fine I. (2013). Neurochemical changes within human early blind occipital cortex. Neuroscience 252, 222–233. 10.1016/j.neuroscience.2013.08.004
    1. Yoshida S., Oishi K., Faria A. V., Mori S. (2013). Diffusion tensor imaging of normal brain development. Pediatr. Radiol. 43, 15–27. 10.1007/s00247-012-2496-x
    1. Zamm A., Schlaug G., Eagleman D. M., Loui P. (2013). Pathways to seeing music: enhanced structural connectivity in colored-music synesthesia. Neuroimage 74, 359–366. 10.1016/j.neuroimage.2013.02.024
    1. Zatorre R. J., Evans A. C., Meyer E. (1994). Neural mechanisms underlying melodic perception and memory for pitch. J. Neurosci. 14, 1908–1919.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다