Vestibular Processing and its Cortical Signature in Humans

The vestibular system encodes rotations and translations of the head in space. While much is known about cortical processing of the classical Aristotelian sensory modalities, such as vision and touch, knowledge of how vestibular stimulation is encoded in the human brain is lacking, probably due to the inherent technical difficulties of recording human brain function while providing natural vestibular stimulation. Here, I used electroencephalography (EEG), psychophysics, and a custom-built rotating chair to elucidate how natural vestibular stimulation is encoded and processed in the brain, and identified novel markers of vestibular processing in the brain in the frequency domain. Specifically, in one set of experiments the spectral response to rotations were analyzed during constant velocity stimulation and short, transient stimulations in healthy subjects and bilateral vestibular-loss patients (BVPs). In another set of experiments the time course of spectral modulations was compared to that of the vestibulo-ocular response (VOR), which decays exponentially during constant velocity rotational stimulation with a time constant of 10-30s. Throughout all EEG experiments, spectral power in the alpha (8-13 Hz) band was found to consistently encode vestibular stimulation. Furthermore, the multisensory nature of the vestibular system was studied statistically by using a Bayes-optimal integration model to better understand how visual and vestibular information are combined in the brain to form a percept. Results across these experiments indicate that visual and vestibular information are not just integrated optimally, but also âfusedâ at the perceptual level.

Visuo-vestibular mechanisms of bodily self-consciousness

Joachim Jean-Marie Forget

Bodily self-consciousness is linked to multisensory integration and is particularly dependent on vestibular perception providing the brain with the main sensory cues about body motion and location in space. Vestibular and visual inputs are permanently balanced and integrated to encode the most optimal representation of the external world and of the observer in the central nervous system. Vection, an illusory self-motion experience induced only by visual stimuli, illustrates the fact that the visual and the vestibular systems share common neural underpinnings and a similar phenomenology. Optokinetic stimulation inducing vection and direct vestibular stimulation induce whole-body motion sensations that can be used to explore multisensory interactions. A failure in visuo-vestibular integration, artificially induced by the methods of cognitive psychology or in pathological conditions, has also been reported to altered own body perception and bodily self-consciousness. The respective contributions of the vestibular and visual systems to bodily self-consciousness amongst other polymodal sensory mechanisms, and the neural correlates of visuo-vestibular convergence, should be better understood. We first performed a neuroimaging study of brain regions where optokinetic and vestibular stimuli converge, using 7T functional magnetic resonance imaging in individual subjects. We identified three main regions of convergence: (1) the depth of supramarginal gyrus or retroinsular cortex, (2) the surface of supramarginal gyrus at the temporo-parietal junction, (3) and the posterior part of middle temporal gyrus and superior temporal sulcus. Then, we aimed to induce the embodiment of an external fake rubber hand through visuo-tactile conflict - the so-called rubber hand illusion paradigm, and studied how this integration is modulated by vection. Subjects experiencing vection in the direction of the rubber hand mislocalised the position of their real hand towards the rubber hand indicating that visuo-vestibular stimuli can enhance visuo-tactile integration. We also investigated if visuo-proprioceptive and tactile integration in peripersonal space could be dynamically updated based on the congruency of visual and proprioceptive feedback. A pair of rubber hands or feet provided visual feedback. Fake and real limbs were crossed or uncrossed. We showed that sensory cues were integrated in peripersonal space, dynamically reshaped but only for hands. Finally, we investigated a rare case of an illusory own body perception in an epileptic patient suffering from multiple daily disembodiments during seizures. Seizures were associated to a focal cortical microdysplasia juxtaposed to a developmental venous anomaly in the left angular gyrus, a brain region known to be important for visuo-vestibular integration and bodily self-consciousness. Our results characterize the inferior parietal lobule as a crucial structure in merging visual, vestibular, tactile and proprioceptive inputs, allowing the emergence of the global and unified experience of being âI.â Multisensory body representation can be reshaped transiently using visual and vestibular signals or in relation to a medical condition affecting the temporo-parietal junction. The integration of visual and vestibular signals, aims to adapt dynamically our internal representations to constant changes occurring in our environment.

EPFL2015

Spike frequency adaptation supports network computations on temporally dispersed information

Anand Subramoney

For solving tasks such as recognizing a song, answering a question, or inverting a sequence of symbols, cortical microcircuits need to integrate and manipulate information that was dispersed over time during the preceding seconds. Creating biologically realistic models for the underlying computations, especially with spiking neurons and for behaviorally relevant integration time spans, is notoriously difficult. We examine the role of spike frequency adaptation in such computations and find that it has a surprisingly large impact. The inclusion of this well-known property of a substantial fraction of neurons in the neocortex - especially in higher areas of the human neocortex - moves the performance of spiking neural network models for computations on network inputs that are temporally dispersed from a fairly low level up to the performance level of the human brain.

ELIFE SCIENCES PUBLICATIONS LTD2021

Spatio-temporal coupling of the electric and hemodynamic brain responses in humans

Roberto Martuzzi

Our comprehension of human brain functions and their dynamics has been dramatically improved by recent developments in non-invasive imaging techniques. These methods can be divided into two different categories, according to the nature of the measured signal: hemodynamic techniques, such as functional magnetic resonance imaging (fMRI) and positiron emission tomography (PET), and electromagnetic techniques, such as electroencephalography (EEG) and magnetoencephalography (MEG). These two categories are have complementary characteristics: hemodynamic techniques have a good spatial resolution (on a millimeter spatial scale) but have a poor temporal resolution, which is inherently limited by the rate changes in blood flow and oxygenation. Electromagnetic techniques have sub-millisecond temporal resolution but have a poor spatial resolution, since the analysis of intracranial generators requires the solution of an underdetermined inverse problem (i.e. there are infinite solutions that can explain equally well the same scalp-recorded distribution). The complementarity of the characteristics of these two families of methods allowed researchers to suppose that the understanding of spatio-temporal brain dynamics can be drastically improved by their combination (so-called multimodal imaging). Unfortunately some caveats hinder such combination. First, the nature of neurovascular coupling is still poorly understood. Second, analytical methods for multimodal imaging are largely in their infancy. The first part of this thesis focuses on the analysis of the temporal characteristics of the blood oxygenation level dependent (BOLD) signal and on how they are modulated by stimulus conditions. To analyze the BOLD dynamics, a novel method for synchronizing stimulus delivery and volume acquisition was developed. This method allows for estimating the BOLD signal with a high temporal resolution (in this thesis up to 125 ms) and for studying how the temporal characteristics (in this thesis mainly the BOLD peak latency and slope) are modulated by stimulus conditions (with an approach similar to that used in the analysis of the EEG evoked potentials). We applied this novel technique to a simple reaction time task to lateralized visual stimuli (the so-called Poffenberger paradigm) as well as to a multisensory auditory-visual reaction time task. In the first study (the Poffenberger paradigm) the analysis of BOLD dynamics supported the theory of a bilateral visuo-motor pathway even in the case of a visual stimulus ipsilateral to the responding hand. In the second study, (the auditory-visual multisensory reaction-time task), the analysis showed auditory-visual interactions within both primary auditory and visual cortices that could not be otherwise revealed by traditional fMRI analysis methods since it does not involve changes in signal amplitude. The second part of this thesis focuses on the comparison of the statistical results obtained by the analyses of fMRI and of the intracranial local field potentials (LFPs), estimated by the ELECTRA inverse solution. We first developed a new method for the analysis of EEG data. This method is based on the statistical comparison of the spectral characteristics of the estimated intracranial LFPs of the pre- and post- stimulus onset periods. Each single trial is analyzed independently, without including an averaging step, so that the information carried by high frequencies is preserved. We also propose a new metric, called resemblance, to investigate the relationship between fMRI and the estimated intracranial LFPs. Single-trial analysis and the resemblance metric were applied in an experiment involving separate EEG and fMRI acquisitions during the same passive visual stimulation protocol. This experiment revealed that only a limited set of LFP frequencies shows a spatial correlation with fMRI. This set of frequencies changes across brain areas, such that progression from lower to higher cortical levels of visual processing incorporates at each step new frequencies. In conclusion, in this thesis we show that the estimation and the analysis of the BOLD time course can give an important contribution to better understanding brain functions and brain organization. To fully understand the meaning of changes in BOLD dynamics, we need a better knowledge of the neuro-vascular coupling. To do that, we introduced a new method for evaluating the relationship between EEG and fMRI across frequencies and anatomical regions.