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Integration of Multiple Simultaneous Stimuli Within and Between Somatosensory Sub-Modalities

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Integration of Multiple Simultaneous Stimuli Within and Between Somatosensory Sub-Modalities Alma Mater Studiorum – Università di Bologna DOTTORATO DI RICERCA IN Joint International PhD Programme in Cognitive Neuroscience Ciclo XXIX Settore Concorsuale di afferenza: 11/E1 Settore Scientifico disciplinare: M-PSI/02 Integration of multiple simultaneous stimuli within and between somatosensory sub-modalities Presentata da: Dott. Antonio Cataldo Coordinatore Dottorato Relatore Prof.ssa Monica Rubini Prof. Giuseppe di Pellegrino Correlatore Prof. Patrick Haggard Esame finale anno 2017 2 Abstract Psychological characterisation of the somatosensory system often focusses on minimal units of perception, such as detection, localisation, and magnitude estimation of single events. Research on how multiple simultaneous stimuli are aggregated to create integrated, synthetic experiences is rarer. Yet, increasing evidence suggests that the somatosensory integration of composite patterns is regulated by nonlinear mechanisms occurring at different stages of the perceptual processing. As a consequence, the bulk of knowledge concerning the perception of isolated events may be insufficient to grasp the complexity of uni- and cross-modal interactions. This thesis aims to shed a light on the mechanisms underlying the integration of multiple simultaneous stimuli, within and between different sub-modalities of the somatosensory system. First, across several psychophysical experiments, we investigated the ability of healthy individuals to perceive the total intensity of composite somatosensory patterns. We found that the overall intensity of tactile, cold, or warm patterns was systematically overestimated when the multiple simultaneous stimuli had different intensities (Chapter 2). Thus, perception of somatosensory totals is biased towards the most salient element in the pattern. Furthermore, we demonstrated that peak-biased aggregation is a genuine perceptual phenomenon which does not rely on the discrimination of the parts, but is rather based on the salience (i.e. the signal-to-noise ratio) of each stimulus (Chapter 3). Next, we studied a classical thermal illusion to assess participants’ ability to localise thermal stimuli delivered on the fingers either in isolation, or in uniform and non-uniform patterns (Chapter 4). We found that despite a surprisingly high accuracy in reporting the 3 location of a single stimulus, when participants were presented with non-uniform patterns, their ability to identify the thermal state of a specific finger was completely abolished. Lastly, we investigated the perceptual and neural correlates of thermo-nociceptive interaction during the presentation of multiple thermal stimuli (Chapter 5). We replicated the classical suppressive effect of warmth on pain. Crucially, we also found that inhibition of pain was independent from both the position and the number of thermal stimuli administered, providing insights about the level of somatosensory processing at which the interaction takes place. Overall, our results suggest that nonlinear integration of multiple stimuli, within and between somatosensory sub-modalities, may be an efficient way by which the somatosensory system synthesises the complexity of reality, providing us with an extended and coherent perception of the world, in spite of its deep bandwidth limitations. 4 Table of contents Abstract ........................................................................................................ 1 List of Figures .............................................................................................. 9 List of Tables .............................................................................................. 13 Chapter 1. From the perception of single events, to the integration of multiple simultaneous somatosensory stimuli ......................................... 15 1.1 Introduction ...................................................................................................... 15 1.1.1 Somatosensation: the most essential and complex of our senses 16 1.1.2 General purpose and structure of the thesis ................................. 23 1.2 Somatosensory processing of single events ..................................................... 24 1.2.1 Perception of tactile stimuli ........................................................... 27 1.2.2 Perception of thermal stimuli ........................................................ 35 1.2.3 Perception of noxious stimuli ........................................................ 39 1.3 Evidence for nonlinear effects of multiple simultaneous stimulation .............. 45 1.3.1 Detection of multiple somatosensory stimuli and lateral inhibition 46 1.3.2 Mislocalisation of multiple somatosensory stimuli ......................... 50 1.3.3 Spatial summation of thermal stimuli ............................................ 53 1.4 Research questions ........................................................................................... 55 1.4.1 Study 1 and 2: perception of the overall intensity of somatosensory patterns 56 1.4.2 Study 3: mislocalisation of warmth during multiple thermal stimulation 58 1.4.3 Study 4: somatosensory interaction between pain and multiple thermal stimuli 60 5 Chapter 2. Salience-driven overestimation of total somatosensory stimulation 63 2.1 Introduction ...................................................................................................... 63 2.2 Methods ............................................................................................................ 68 2.2.1 Experiment 1 ................................................................................ 69 2.2.2 Experiment 2 ................................................................................ 75 2.2.3 Experiment 3 ................................................................................ 77 2.2.4 Experiment 4 ................................................................................ 78 2.3 Results ............................................................................................................... 81 2.3.1 Experiment 1 ................................................................................ 81 2.3.2 Experiment 2 ................................................................................ 83 2.3.3 Experiment 3 ................................................................................ 86 2.3.4 Experiment 4 ................................................................................ 88 2.4 Discussion .......................................................................................................... 90 Chapter 3. When all is more than the sum of its parts: integration of multiple discrepant tactile stimuli ............................................................. 99 3.1 Introduction ...................................................................................................... 99 3.2 Methods .......................................................................................................... 106 3.2.1 Experiment 1 .............................................................................. 106 3.2.2 Experiment 2 .............................................................................. 110 3.2.3 Experiment 3 .............................................................................. 113 3.3 Results ............................................................................................................. 117 3.3.1 Experiment 1 .............................................................................. 117 3.3.2 Experiment 2 .............................................................................. 119 3.3.3 Experiment 3 .............................................................................. 122 3.4 Discussion ........................................................................................................ 123 6 Chapter 4. Thermal referral: evidence for a thermoceptive uniformity illusion without touch ........................................................................................... 141 4.1 Introduction .................................................................................................... 141 4.2 Methods .......................................................................................................... 144 4.2.1 Experiment 1 .............................................................................. 149 4.2.2 Experiment 2 .............................................................................. 151 4.2.3 Experiment 3 .............................................................................. 152 4.3 Results ............................................................................................................. 153 4.3.1 Experiment 1 .............................................................................. 153 4.3.2 Experiment 2 .............................................................................. 157 4.3.3 Experiment 3 .............................................................................. 159 4.4 Discussion ........................................................................................................ 161 Chapter 5. Thermo-nociceptive interaction: inter-channel pain modulation occurs before intra-channel convergence of warmth .......................... 171 5.1 Introduction .................................................................................................... 171 5.2 Methods .......................................................................................................... 179 5.2.1 Experiment
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