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Nonlinear encoding of sounds in the auditory cortex

  • Kempf, Alexandre
Publication Date
Oct 17, 2018
Kaleidoscope Open Archive
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Perceptual objects are the elementary units used by the brain to construct an inner world representation of the environment from multiple physical sources, like light or sound waves. While the physical signals are first encoded by receptors in peripheral organs into neuroelectric signals, the emergence of perceptual object require extensive processing in the central nervous system which is not yet fully characterized. Interestingly, recent advances in deep learning shows that implementing series of nonlinear and linear operations is a very efficient way to create models that categorize visual and auditory perceptual objects similarly to humans. In contrast, most of the current knowledge about the auditory system concentrates on linear transformations. In order to establish a clear example of the contribution of auditory system nonlinearities to perception, we studied the encoding of sounds with an increasing intensity (up ramps) and a decreasing intensity (down ramps) in the mouse auditory cortex. Two behavioral tasks showed evidence that these two sounds are perceived with unequal salience despite carrying the same physical energy and spectral content, a phenomenon incompatible with linear processing. Recording the activity of large cortical populations for up- and down-ramping sounds, we found that cortex encodes them into distinct sets of non-linear features, and that asymmetric feature selection explained the perceptual asymmetry. To complement these results, we also showed that, in reinforcement learning models, the amount of neural activity triggered by a stimulus (e.g. a sound) impacts learning speed and strategy. Interestingly very similar effects were observed in sound discrimination behavior and could be explain by the amount of cortical activity triggered by the discriminated sounds. This altogether establishes that auditory system nonlinearities have an impact on perception and behavior. To more extensively identify the nonlinearities that influence sounds encoding, we then recorded the activity of around 60,000 neurons sampling the entire horizontal extent of auditory cortex. Beyond the fine scale tonotopic organization uncovered with this dataset, we identified and quantified 7 nonlinearities. We found interestingly that different nonlinearities can interact with each other in a non-trivial manner. The knowledge of these interactions carry good promises to refine auditory processing model. Finally, we wondered if the nonlinear processes are also important for multisensory integration. We measured how visual inputs and sounds combine in the visual and auditory cortex using calcium imaging in mice. We found no modulation of supragranular auditory cortex in response to visual stimuli, as observed in previous others studies. We observed that auditory cortex inputs to visual cortex affect visual responses concomitant to a sound. Interestingly, we found that auditory cortex projections to visual cortex preferentially channel activity from neurons encoding a particular non-linear feature: the loud onset of sudden sounds. As a result, visual cortex activity for an image combined with a loud sound is higher than for the image alone or combine with a quiet sound. Moreover, this boosting effect is highly nonlinear. This result suggests that loud sound onsets are behaviorally relevant in the visual system, possibly to indicate the presence of a new perceptual objects in the visual field, which could represent potential threats. As a conclusion, our results show that nonlinearities are ubiquitous in sound processing by the brain and also play a role in the integration of auditory information with visual information. In addition, it is not only crucial to account for these nonlinearities to understand how perceptual representations are formed but also to predict how these representations impact behavior.

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