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Temporal Structure of Perception and Neuronal Stimulus Processing

Periodic Reporting for period 2 - TeSP (Temporal Structure of Perception and Neuronal Stimulus Processing)

Reporting period: 2020-05-01 to 2021-04-30

Neuroscientific studies usually investigate perception as an event that occurs at a particular isolated time point. Specifically, most studies analyze how the brain reacts to the presentation of a single stimulus, which is then repeated identically across multiple trials. This approach ignores, however, two important factors that are known to significantly influence perception and neural processing of sensory information:
First, in natural environments, stimuli are almost never presented in isolation. Instead, they are embedded into certain temporal or spatial contexts. The contexts are full of regularities, which contain information predicting what kind of sensory information to expect next. In other words, your brain “predicts” which future sensory input is most likely, based on the kind of sensory input it received in the past. Therefore, if we exclusively study how the brain processes single stimuli void of any context, we overlook a fundamental component of perception.
Second, recent studies have demonstrated that perception across different sensory modalities is systematically influenced by ongoing neural activity patterns, which occur already before the presentation of the investigated stimulus. Thus, the ever-changing state of our brain systematically influences how we will perceive any upcoming sensory information. Consequently, if scientific analysis focuses exclusively the time during and after stimulus presentation, such “pre-stimulus” states and their influence on neural stimulus processing and perception will be overlooked.
Consequently, the current challenge of perceptual neuroscience is to devise experimental paradigms and analysis techniques that acknowledge the dependence of perception on contextual factors and of neural stimulus processing to ongoing brain activity fluctuations. By adopting a holistic perspective, the present project will elucidate how the brain performs the active process of perception and how this process relies on both contextual sensory information and ever-changing brain states.
The current project aims to overcome the above-mentioned limitations by studying how perception and neural processing of stimuli is influenced by past sensory information that contains predictive information and by determining markers of ongoing brain activity relevant for perception. Specifically, this project investigates how the brain determines what past sensory information is taken into account to form predictions about probable future sensory input, thereby providing valuable insights into the temporal structure of perception.
From the clinical perspective, the current project studies alterations in ongoing neural activity in patients with Hepatic Encephalopathy, a brain disease caused by liver failure. Patients with HE usually have systematic perceptual impairments, specifically in the temporal dimension. This project highlights markers of ongoing neural activity underlying the temporal organization of stimulus processing and perception and investigates if these markers indicate the individual disease state.
The present project demonstrated that the human brain integrates past contextual information in order to predict what sensory information probably will appear next. This integration happens across a discrete number of past stimuli, instead of being linked to a specific duration. This mechanism allows for a flexible reaction to sensory input presented at different speed, since neural integration flexible scales depending on presentation speed.
Regarding ongoing neural activity changes and their connection to perceptual impairments in Hepatic Encephalopathy (HE), the current action revealed that the known visual impairments in HE are linked to decreases of the dominant frequency of ongoing oscillatory neural activity. Aside from their visual impairments, HE patients also exhibit similar impairments in the tactile domain. A possible reason for neural alterations in HE lies in the reduced synaptic plasticity in cortical areas.
During the outgoing phase (June 2018 - June 2020), the recruited researcher performed an MEG study using a novel auditory prediction paradigm. The resulting key publication (Baumgarten et al., Nature Communications, 2021) answers the question of how the human brain deals with the challenge that incoming sensory information is often presented at a different speed. In other words, how is it that we can understand both a very fast and a very slow speaker? The present work demonstrates that the brain integrates past sensory information similarly over a certain range of presentation speeds (i.e. up to the factor 4) by accumulating past sensory information over a specific amount of information (e.g. over the last 7 tones), instead of integrating over a fixed period of time (e.g. the last 5 seconds). The brain then uses this information to predict which tone most likely appears next. Since these results are based on a paradigm using stimuli that have similar statistics as natural stimuli, the underlying neural mechanisms can be generalized to everyday situations. Using intracranial ECoG recordings in epileptic patients, the recruited researcher further demonstrated that the integration of past sensory information happens distributed across the brain, whereas the processes of predicting the most likely next tones happens mostly in around sensory areas.
In collaboration with the European beneficiary, the recruited researcher has published two papers on the temporal resolution of sensory perception and the underlying neural mechanisms in patients with Hepatic Encephalopathy (HE). The first publication (Baumgarten et al., NeuroImage Clinical, 2018) demonstrated that the dominant frequency of oscillatory neural activity in the alpha-band (~8-12 Hz) is linked to the perceptual resolution of visual perception. Notably, both a reduction in the dominant frequency and an impaired temporal resolution of visual perception is found in patients with HE. Further, the recruited researcher collaborated on a study demonstrating that the known visual impairments of patients with HE are paralleled by similar temporal impairments in the tactile domain (Lazar, ... Baumgarten, et al. Frontiers in Psychology, 2018), which provides an additional behavioral parameter to rate individual disease state.
During the return period (December 2020 - November 2021), the recruited researcher demonstrated that the alterations in neural functioning in HE patients arise as consequences of a reduced synaptic plasticity in cortical areas (Nikolov*, Baumgarten*, et al., Clinical Neurophysiology, 2021; *shared first authorship). He currently investigates the neural correlates of the abovementioned impaired tactile perception in HE.
The present project substantially adds to the current state of the art in perceptual neuroscience. Especially its generation of a paradigm implementing predictive information in a way it is present in natural settings and the corresponding results are of importance to the field. Further, the unambiguous localization and distinction of the neural mechanisms underlying the integration and prediction of sensory information by means of ECoG opens up promising avenues for future basic and clinical research. Regarding the clinical work, the current project successfully brought basic neuroscientific findings to clinical use.
Hypotheses of Baumgarten et al., 2021
Stimulus sequences used in Baumgarten et al., 2021