Bayesian surprise shapes neural responses in somatosensory cortical circuits
Gwendolyn English,
Newsha Ghasemi Nejad,
Marcel Sommerfelt,
Mehmet Fatih Yanik,
Wolfger von der Behrens
Affiliations
Gwendolyn English
Institute of Neuroinformatics, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; ZNZ Neuroscience Center Zurich, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; Corresponding author
Newsha Ghasemi Nejad
Institute of Neuroinformatics, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; ZNZ Neuroscience Center Zurich, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland
Marcel Sommerfelt
Institute of Neuroinformatics, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland
Mehmet Fatih Yanik
Institute of Neuroinformatics, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; ZNZ Neuroscience Center Zurich, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland
Wolfger von der Behrens
Institute of Neuroinformatics, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; ZNZ Neuroscience Center Zurich, ETH Zurich & University of Zurich, 8057 Zurich, Switzerland; Corresponding author
Summary: Numerous psychophysical studies show that Bayesian inference governs sensory decision-making; however, the specific neural circuitry underlying this probabilistic mechanism remains unclear. We record extracellular neural activity along the somatosensory pathway of mice while delivering sensory stimulation paradigms designed to isolate the response to the surprise generated by Bayesian inference. Our results demonstrate that laminar cortical circuits in early sensory areas encode Bayesian surprise. Systematic sensitivity to surprise is not identified in the somatosensory thalamus, rather emerging in the primary (S1) and secondary (S2) somatosensory cortices. Multiunit spiking activity and evoked potentials in layer 6 of these regions exhibit the highest sensitivity to surprise. Gamma power in S1 layer 2/3 exhibits an NMDAR-dependent scaling with surprise, as does alpha power in layers 2/3 and 6 of S2. These results show a precise spatiotemporal neural representation of Bayesian surprise and suggest that Bayesian inference is a fundamental component of cortical processing.