Common Phenomenal and Neural Substrate Geometry in Visual Motion Perception.

Abstract

What is a possible physical substrate of the qualitative aspects of consciousness (qualia)? Answering this question is a central goal of consciousness research. Due to their subjective and ineffable nature, finding a quantitative way to characterise qualia from verbal description has thus far proven elusive. To overcome the challenge of expressing subjective experience, recent structural and relational approaches have been proposed from mathematics. Yet, as far as we know, no attempts have been made to evaluate the relationship between a certain structure of qualia and the structure of a candidate underlying physical substrate. Towards this ambitious goal of linking the structures of qualia and physical, we set out to make an empirical first step by focusing on experienced dissimilarity of visual motion in human participants and stimulus-evoked neural population response geometry recorded from mouse primary visual cortex. From human participants (N=171), we obtained dissimilarity ratings of visual motion experiences induced by 48 stimuli, spanning across 8 directions and 6 spatial frequencies. Analysis revealed a human dissimilarity structure that was not well captured by a simple monotonic function of physical motion-direction difference alone nor by a pure orientation-symmetry account. From nine individual mice, we recorded single-neuron activity (n=751) with optical imaging in both awake and lightly anaesthetised conditions (isoflurane 0.6-0.8%). From neuron population responses to a similar set of motion stimuli, we computed a distance matrix that is comparable to our human dissimilarity matrix. Quantitative analyses show structural commonalities between a human dissimilarity structure and mouse neural structure, where a categorical organisation of stimulus direction best explained both. These commonalities were similar in awake and anaesthetised recordings, suggesting that this coarse V1 geometry is relatively insensitive to this type of anaesthesia; future work combining behaviour with causal intervention is required to relate such neural structures to conscious experience. Finally, we list several empirical factors that can be improved to promote our qualia structure approach in the future. Graphical AbstractSimilarity structures derived from a pairwise similarity rating task in humans revealed a mismatch between physical stimuli and subjective experience of similarity of visual motion: participants robustly rated their experience of opposite direction stimuli as similar. In mice, we used 2-photon Ca2+ imaging to record the activity of c.80 neurons per mouse in the primary visual cortex (V1) of nine mice. By computing a correlation matrix that records the similarity of responses to the same pairwise comparisons as in humans across all neurons, we can then represent neuronal distance. This revealed that mice neurons also exhibited the same dissociation between physical stimuli and responses as in humans at lower spatial frequencies. By comparing these dissimilarity and distance matrices using linear mixed effects modelling, we showed that a categorical model, not direction or orientation, best explains both human and mice data. Ultimately, this study is a methodological proof-of-concept for comparing structures of experience to candidate structures of a possible neural substrate in order to constrain their candidacy. O_FIG O_LINKSMALLFIG WIDTH=195 HEIGHT=200 SRC="FIGDIR/small/679834v2_ufig1.gif" ALT="Figure 1"> View larger version (73K): org.highwire.dtl.DTLVardef@768e3forg.highwire.dtl.DTLVardef@174e501org.highwire.dtl.DTLVardef@166cf75org.highwire.dtl.DTLVardef@be1a6e_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIVisual motion feels more similar for opposite than diagonal directions C_LIO_LIPairwise similarity ratings reveal structure of visual motion experience C_LIO_LIHuman motion experience and mouse visual cortex share a common geometry C_LIO_LIMouse visual cortex codes motion similarly when awake and lightly anaesthetised C_LI