Abstract

Objective: Traditional theories in neuroscience state that tactile afferents present in the glabrous skin of the human hand encode tactile information following a submodality segregation strategy, meaning that each modality (eg. motion, vibration, shape, ... ) is encoded by a different afferent class. Modern theories suggest a submodality convergence instead, in which different afferent classes work together to capture information about the environment through tactile sense. Typically, studies involve electrophysiological recordings of tens of afferents. At the same time, the human hand is filled with around 17.000 afferents. In this thesis, we want to tackle the theoretical gap this poses. Specifically, we aim to address whether the peripheral nervous system relies on population coding to represent tactile information and whether such population coding enables us to disambiguate submodality convergence against the classical segregation. Approach: Understanding the encoding and flow of information in the nervous system is one of the main challenges of modern neuroscience. Neural signals are highly variable and may be non-linear. Moreover, there exist several candidate codes compatible with sensory and behavioral events. For example, they can rely on single cells or populations and also on rate or timing precision. Information-theoretic methods can capture non-linearities while being model independent, statistically robust, and mathematically well-grounded, becoming an ideal candidate to design pipelines for analyzing neural data. Despite information-theoretic methods being powerful for our objective, the vast majority of neural signals we can acquire from living systems makes analyses highly problem-specific. This is so because of the rich variety of biological processes that are involved (continuous, discrete, electrical, chemical, optical, ...). Main results: The first step towards solving the aforementioned challenges was to have a solid methodology we could trust and rely on. Consequently, the first deliverable from this thesis is a toolbox that gathers classical and state-of-the-art information-theoretic approaches and blends them with advanced machine learning tools to process and analyze neural data. Moreover, this toolbox also provides specific guidance on calcium imaging and electrophysiology analyses, encompassing both simulated and experimental data. We then designed an information-theoretic pipeline to analyze large-scale simulations of the tactile afferents that overcomes the current limitations of experimental studies in the field of touch and the peripheral nervous system. We dissected the importance of population coding for the different afferent classes, given their spatiotemporal dynamics. We also demonstrated that different afferent classes encode information simultaneously about very simple features, and that combining classes increases information levels, adding support to the submodality convergence theory. Significance: Fundamental knowledge about touch is essential both to design human-like robots exhibiting naturalistic exploration behavior and prostheses that can properly integrate and provide their user with relevant and useful information to interact with their environment. Demonstrating that the peripheral nervous system relies on heterogeneous population coding can change the designing paradigm of artificial systems, both in terms of which sensors to choose and which algorithms to use, especially in neuromorphic implementations.

Publications

Corniani, G., Casal, M. A., Panzeri, S., & Saal, H. P. (2022). Population coding strategies in human tactile afferents. PLOS Computational Biology, 18(12), e1010763.

Maffulli, R., Casal, M. A., Celotto, M., Zucca, S., Safaai, H., Fellin, T., & Panzeri, S. (2022). NIT: an open-source tool for information theoretic analysis of neural population data. bioRxiv, 2022-12.