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Not all predictions are equal: "What" and "when" predictions modulate activity in auditory cortex through different mechanisms

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Auksztulewicz,  Ryszard
Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London;
Department of Neuroscience, Max Planck Institute for Empirical Aesthetics, Max Planck Society;
Department of Biomedical Sciences, City University of Hong Kong;

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Melloni,  Lucia
Department of Neuroscience, Max Planck Institute for Empirical Aesthetics, Max Planck Society;
Department of Neurology, NYU Langone Medical Center;

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Citation

Auksztulewicz, R., Schwiedrzik, C. M., Thesen, T., Doyle, W., Devinsky, O., Nobre, A. C., et al. (2018). Not all predictions are equal: "What" and "when" predictions modulate activity in auditory cortex through different mechanisms. The Journal of Neuroscience, 38(40), 8680-8693. doi:10.1523/JNEUROSCI.0369-18.2018.


Cite as: http://hdl.handle.net/21.11116/0000-0002-7376-8
Abstract
Using predictions based on environmental regularities is fundamental for adaptive behavior. While it is widely accepted that predictions across different stimulus attributes (e.g., time and content) facilitate sensory processing, it is unknown whether predictions across these attributes rely on the same neural mechanism. Here, to elucidate the neural mechanisms of predictions, we combine invasive electrophysiological recordings (human electrocorticography in 4 females and 2 males) with computational modeling while manipulating predictions about content ("what") and time ("when"). We found that "when" predictions increased evoked activity over motor and prefrontal regions both at early (similar to 180 ms) and late (430 - 450 ms) latencies. "What" predictability, however, increased evoked activity only over prefrontal areas late in time (420 - 460 ms). Beyond these dissociable influences, we found that "what" and "when" predictability interactively modulated the amplitude of early (165 ms) evoked responses in the superior temporal gyrus. We modeled the observed neural responses using biophysically realistic neural mass models, to better understand whether "what" and "when" predictions tap into similar or different neurophysiological mechanisms. Our modeling results suggest that "what" and "when" predictability rely on complementary neural processes: "what" predictions increased short-term plasticity in auditory areas, whereas "when" predictability increased synaptic gain in motor areas. Thus, content and temporal predictions engage complementary neural mechanisms in different regions, suggesting domain-specific prediction signaling along the cortical hierarchy. Encoding predictions through different mechanisms may endow the brain with the flexibility to efficiently signal different sources of predictions, weight them by their reliability, and allow for their encoding without mutual interference.