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Premio Tesi Di Dottorato – 38 – PREMIO TESI DI DOTTORATO Commissione Giudicatrice, Anno 2013 premio tesi di dottorato – 38 – PREMIO TESI DI DOTTORATO Commissione giudicatrice, anno 2013 Luigi Lotti, presidente della Commissione Tito Arecchi, Area Scientifica Franco Cambi, Area Umanistica Paolo Felli, Area Tecnologica Michele Arcangelo Feo, Area Umanistica Roberto Genesio, Area Tecnologica Luigi Lotti, Area Scienze Sociali Mario Pio Marzocchi, Area Scientifica Adolfo Pazzagli, Area Biomedica Mario Giuseppe Rossi, Area Umanistica Salvatore Ruggieri, Area Biomedica Saulo Sirigatti, Area Biomedica Piero Tani, Area Scienze Sociali Fiorenzo Cesare Ugolini, Area Tecnologica Vincenzo Varano, Area Scienze Sociali Graziella Vescovini, Area Umanistica Claudia Lunghi Early cross-modal interactions and adult human visual cortical plasticity revealed by binocular rivalry Firenze University Press 2014 Early cross-modal interactions and adult human visual cortical plasticity revealed by binocular rivalry / Claudia Lunghi. – Firenze : Firenze University Press, 2014. (Premio Tesi di Dottorato; 38) http://digital.casalini.it/9788866556879 ISBN 978-88-6655-686-2 (print) ISBN 978-88-6655-687-9 (online) Cover image: © Stuart Miles | Dreamstime.com Peer Review Process All publications are submitted to an external refereeing process under the responsibility of the FUP Editorial Board and the Scientific Committees of the individual series. The works published in the FUP catalogue are evaluated and approved by the Editorial Board of the publishing house. For a more detailed description of the refereeing process we refer to the official documents published in the online catalogue of the FUP (www.fupress.com). Firenze University Press Editorial Board G. Nigro (Co-ordinator), M.T. Bartoli, M. Boddi, R. Casalbuoni, C. Ciappei, R. Del Punta, A. Dolfi, V. Fargion, S. Ferrone, M. Garzaniti, P. Guarnieri, A. Mariani, M. Marini, A. Novelli, M. Verga, A. Zorzi. This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0: http://creativecommons.org/licenses/by/4.0/) CC 2014 Firenze University Press Università degli Studi di Firenze Firenze University Press Borgo Albizi, 28, 50122 Firenze, Italy www.fupress.com Printed in Italy Table of contents Abstract 7 Chapter 1 General Introduction 9 1.1. What is Binocular Rivalry? 9 1.2. What rivals during binocular rivalry? Eye versus Stimulus Rivalry. 13 1.3. Binocular Rivalry dynamics. 18 1.3.1. Phase duration distribution 19 1.3.2. Stimulus strength and the dynamics of binocular rivalry 20 1.3.3 Onset Rivalry 22 1.4. Binocular Rivalry Suppression 24 1.4.1 Visual adaptation and priming to suppressed patterns 25 1.4.2. Where does suppression take place in the visual brain? 28 1.5. Binocular Rivalry and Attention. 32 1.5.1. Voluntary/Endogenous attention and binocular rivalry 34 1.5.2. Involuntary/Exogenous attention and binocular rivalry 37 1.5.3. Is attention necessary for binocular rivalry? 38 Chapter 2 Cross-modal interactions during binocular rivalry 41 2.1. Introduction. Multisensory Processing. 41 2.1.1. Multisensory processing in the superior colliculus (SC). 41 2.1.2. Multisensory Integration in temporal and parietal cortical areas. 43 2.1.3. Cross-modal interactions in (previously thought) unisensory areas. 44 2.1.4. Maximum Likelihood Estimation model of multisensory integration. 47 2.1.5. Cross-modal interactions and bistable perception 48 2.2. Touch interacts with binocular rivalry at early stages of visual processing. 50 2.2.1. Touch specifically interferes with the dynamics of binocular rivalry 51 2.2.2. The interaction between vision and touch during binocular rivalry is strictly tuned for orientation 57 Claudia Lunghi, Early cross-modal interactions and adult human visual cortical plasticity revealed by binocular rivalry ISBN 978-88-6655-686-2 (print) ISBN 978-88-6655-687-95 (online), CC BY 4.0, 2014 Firenze University Press Early cross-modal interactions and adult human visual cortical plasticity 2.2.3. Spatial proximity is crucial, active exploration is not. 68 Abstract 2.2.4. Summary and Conclusions 78 Chapter 3 Plasticity of adult human visual cortex revealed by binocular rivalry. 81 3.1. Introduction 81 3.1.1. Juvenile plasticity of the visual system: the critical period. 81 3.1.2. Visual cortical plasticity in the adult. 87 3.2. Brief periods of monocular deprivation disrupt ocular balance in human adult visual cortex. 110 When two incompatible images are contemporaneously displayed to homolo- 3.2.1. Results and Discussion 110 gous portions of the two retinae normal binocular fusion fails, and conscious per- 3.3. Long-term effects of monocular deprivation revealed with binocular rivalry ception continuously oscillates between the two alternatives despite the constant ret- inal stimulation. This unique form of bistable visual perception is called binocular gratings modulated in luminance and in color 115 rivalry, and is a peculiar visual phenomenon that engages competition between mo- 3.3.1. Materials and Methods 116 nocular signals and neural representations of the two images at different levels of 3.3.2. Results 118 visual processing, from LGN to object-selective infero-temporal cerebral areas. Here we present several experiments in which we have used binocular rivalry as a tool to 3.3.3. Discussion 127 investigate different aspects of visual and multisensory perception. 3.3.4. Conclusions 130 In the first set of studies we demosntrated that touch specifically interacts with 3.4. Summary and Conclusions. 130 vision during binocular rivalry and that the interaction likely occurs at early stages of visual processing, probably V1 or V2. We found in fact that touching an engraved Chapter 4 grating interfered with the dynamics of binocular rivalry both by prolonging domi- Binocular Rivalry as a tool to monitor visual system plasticity during occlusion nance and by curtailing suppression of the congruent visual stimulus (parallel grat- therapy in amblyopic children 133 ing). We further demonstrated that the interaction between vision and touch during binocular rivalry was tightly tuned for matched visuo-haptic spatial frequencies and 4.1. Introduction 133 orientations. We finally showed that voluntary attention, action and proprioception 4.1.1. Amblyopia 133 do not play a leading role in mediating the interaction between vision and touch 4.1.2. Occlusion Therapy 134 during rivalry, while spatial and temporal proximity between the visual and the hap- tic stimuli are necessary conditions for the interaction to occur. 4.2. Binocular Rivalry during occlusion therapy 135 In the second set of studies we demonstrated that human adult visual cortex re- 4.2.1. Materials and Methods 135 tains an unexpected high degree of experience-dependent plasticity by showing that 4.2.2. Preliminary results 137 a brief period of monocular deprivation produced important perceptual conse- quences on the dynamics of binocular rivalry, causing the previously deprived eye to 4.2.3. Discussion 139 dominate rivalrous visual perception twice as long as the non-deprived eye. We also found that the effects of monocular deprivation were more long-lasting when visual Chapter 5 stimuli modulated in chromaticity compared to luminance-modulated stimuli were General Conclusions 141 tested, a result suggesting that chromatic vision retains a higher plastic potential. Fi- nally, by showing that monocular deprivation also resulted in stimuli presented to References 143 the deprived eye appearing higher in contrast compared to stimuli presented to the non-deprived eye, we suggest that the perceptual advantage of the deprived eye dur- ing binocular rivalry measured after a short period of monocular deprivation reflects a compensatory homeostatic up-regulation of contrast gain control mechanisms that could be the first reaction of the visual system to the lack of information caused by deprivation. 6 7 Abstract When two incompatible images are contemporaneously displayed to homolo- gous portions of the two retinae normal binocular fusion fails, and conscious per- ception continuously oscillates between the two alternatives despite the constant ret- inal stimulation. This unique form of bistable visual perception is called binocular rivalry, and is a peculiar visual phenomenon that engages competition between mo- nocular signals and neural representations of the two images at different levels of visual processing, from LGN to object-selective infero-temporal cerebral areas. Here we present several experiments in which we have used binocular rivalry as a tool to investigate different aspects of visual and multisensory perception. In the first set of studies we demosntrated that touch specifically interacts with vision during binocular rivalry and that the interaction likely occurs at early stages of visual processing, probably V1 or V2. We found in fact that touching an engraved grating interfered with the dynamics of binocular rivalry both by prolonging domi- nance and by curtailing suppression of the congruent visual stimulus (parallel grat- ing). We further demonstrated that the interaction between vision and touch during binocular rivalry was tightly tuned for matched visuo-haptic spatial frequencies and orientations. We finally showed that voluntary attention, action and proprioception do not play a leading role in mediating the interaction between vision and touch during rivalry, while spatial and temporal proximity between the visual and the hap- tic stimuli are necessary conditions for the interaction to occur. In the second set of studies we demonstrated that human adult visual cortex re- tains
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