Neural Underpinnings of Walking Under Cognitive and Sensory Load: A Mobile Brain/Body Imaging Approach

Dual-task walking studies, in which individuals engage in an attentionally-demanding task while walking, have provided indirect evidence via behavioral and biomechanical measures, of the recruitment of higher-level cortical resources during gait. Additionally, recent EEG and imaging (PET, fNIRS) studies have revealed direct neurophysiological evidence of cortical contributions to steady-state walking. However, there remains a lack of knowledge regarding the underlying neural mechanisms involved in the allocation of cortical resources while walking under increased load. This dissertation presents three experiments designed to provide a greater understanding of the cortical dynamics implicated in processing load (top-down or bottom-up) during locomotion. Furthermore, we seek to investigate age-related differences in these neural pathways. These studies were conducted using an innovative EEG-based Mobile Brain/Body Imaging (MoBI) approach, combining high-density EEG, foot force sensors and 3D body motion capture as participants walked on a treadmill. The first study employed a Go/No-Go response inhibition task to evaluate the long-term test-retest reliability of two cognitively-evoked event-related potentials (ERPs), the earlier N2 and the later P3. Acceptable levels of reliability were found, according to the intraclass correlation coefficient (ICC), and these were similar across sitting and walking conditions. Results indicate that electrocortical signals obtained during walking are stable indices of neurophysiological function. The aim of the second study was to characterize age-related changes in gait and in the allocation of cognitive control under single vs. dual-task load. For young adults, we observed significant modulations as a result of increased task load for both gait (longer stride time) and for ERPs (decreased N2 amplitude and P3 latency). In contrast, older adults exhibited costs in the cognitive domain (reduced accuracy performance), engaged in a more stereotyped pattern of walking, and showed a general lack of ERP modulation while walking under increased load, all of which may indicate reduced flexibility in resource allocation across tasks. Finally, the third study assessed the effects of sensory (optic flow and visual perturbations) and cognitive load (Go/No-Go task) manipulations on gait and cortical neuro-oscillatory activity in young adults. While walking under increased load, participants adopted a more conservative pattern of gait by taking shorter and wider strides, with cognitive load in particular associated with reduced motor variability. Using an Independent Component Analysis (ICA) and dipole-fitting approach, neuro-oscillatory activity was then calculated from eight source-localized clusters of Independent Components (ICs). Significant modulations in average spectral power in the theta (3-7Hz), alpha (8-12Hz), beta (13-30Hz), and gamma (31-45Hz) frequency bands were observed over occipital, parietal and frontal clusters of ICs, as a function of optic flow and task load. Overall, our findings demonstrate the reliability and feasibility of the MoBI approach to assess electrocortical activity in dual-task walking situations, and may be especially relevant to older adults who are less able to flexibly adjust to ongoing cognitive and sensory demands while walking

Cognitive Load Reduces the Effects of Optic Flow on Gait and 2 Electrocortical Dynamics During Treadmill Walking 3

While navigating complex environments the brain must continuously adapt to both external demands such as fluctuating sensory inputs, as well as internal demands, such as engagement in a cognitively demanding task. Previous studies have demonstrated changes in behavior and gait with increased sensory and cognitive load, but the underlying cortical mechanisms remain largely unknown. Here, in a Mobile Brain/Body Imaging (MoBI) approach sixteen young adults walked on a treadmill with high-density EEG while 3D motion capture tracked kinematics of the head and feet. Visual load was manipulated with the presentation of optic flow with and without continuous mediolateral perturbations. The effects of cognitive load were assessed by the performance of a Go/No-Go task on half of the blocks. During increased sensory load, participants walked with shorter and wider strides, which may indicate a more restrained pattern of gait. Interestingly, cognitive task engagement attenuated these effects of sensory load on gait. Using an Independent Component Analysis and dipole-fitting approach, we found that cautious gait was accompanied by neuro-oscillatory modulations localized to frontal (supplementary motor area, anterior cingulate cortex) and parietal (inferior parietal lobule, precuneus) areas. Our results show suppression in alpha/mu (8-12Hz) and beta (13-30Hz) rhythms, suggesting enhanced activation of these regions with unreliable sensory inputs. These findings provide insight into the neural correlates of gait adaptation, and may be particularly relevant to older adults who are less able to adjust to ongoing cognitive and sensory demands while walking

Mobile brain/body imaging of landmark-based navigation with high-density EEG.

Coupling behavioral measures and brain imaging in naturalistic, ecological conditions is key to comprehend the neural bases of spatial navigation. This highly integrative function encompasses sensorimotor, cognitive, and executive processes that jointly mediate active exploration and spatial learning. However, most neuroimaging approaches in humans are based on static, motion-constrained paradigms and they do not account for all these processes, in particular multisensory integration. Following the Mobile Brain/Body Imaging approach, we aimed to explore the cortical correlates of landmark-based navigation in actively behaving young adults, solving a Y-maze task in immersive virtual reality. EEG analysis identified a set of brain areas matching state-of-the-art brain imaging literature of landmark-based navigation. Spatial behavior in mobile conditions additionally involved sensorimotor areas related to motor execution and proprioception usually overlooked in static fMRI paradigms. Expectedly, we located a cortical source in or near the posterior cingulate, in line with the engagement of the retrosplenial complex in spatial reorientation. Consistent with its role in visuo-spatial processing and coding, we observed an alpha-power desynchronization while participants gathered visual information. We also hypothesized behavior-dependent modulations of the cortical signal during navigation. Despite finding few differences between the encoding and retrieval phases of the task, we identified transient time-frequency patterns attributed, for instance, to attentional demand, as reflected in the alpha/gamma range, or memory workload in the delta/theta range. We confirmed that combining mobile high-density EEG and biometric measures can help unravel the brain structures and the neural modulations subtending ecological landmark-based navigation

Mobile brain/body imaging of landmark‐based navigation with high‐density EEG

Coupling behavioral measures and brain imaging in naturalistic, ecological conditions is key to comprehend the neural bases of spatial navigation. This highly integrative function encompasses sensorimotor, cognitive, and executive processes that jointly mediate active exploration and spatial learning. However, most neuroimaging approaches in humans are based on static, motion-constrained paradigms and they do not account for all these processes, in particular multisensory integration. Following the Mobile Brain/Body Imaging approach, we aimed to explore the cortical correlates of landmark-based navigation in actively behaving young adults, solving a Y-maze task in immersive virtual reality. EEG analysis identified a set of brain areas matching state-of-the-art brain imaging literature of landmark-based navigation. Spatial behavior in mobile conditions additionally involved sensorimotor areas related to motor execution and proprioception usually overlooked in static fMRI paradigms. Expectedly, we located a cortical source in or near the posterior cingulate, in line with the engagement of the retrosplenial complex in spatial reorientation. Consistent with its role in visuo-spatial processing and coding, we observed an alpha-power desynchronization while participants gathered visual information. We also hypothesized behavior-dependent modulations of the cortical signal during navigation. Despite finding few differences between the encoding and retrieval phases of the task, we identified transient time-frequency patterns attributed, for instance, to attentional demand, as reflected in the alpha/gamma range, or memory workload in the delta/theta range. We confirmed that combining mobile high-density EEG and biometric measures can help unravel the brain structures and the neural modulations subtending ecological landmark-based navigation

Neural Correlates of Human Cognition in Real-World Environments

According to embodied accounts of human cognition, the mind is at the interface of the body and the environment. For practical reasons, however, neuroscientific research on human cognition has mostly been confined to the laboratory until now. The emergence of portable brain and body imaging research methods offers an unprecedented opportunity to capture the expression of cognitive processes during active behaviours performed in real-world contexts. In the present thesis, electroencephalography (EEG) was used to investigate embodied aspects of human cognition in motion and in the real-world. This approach, however, presents new challenges in terms of signal processing because of the increased noise related to whole body movements. As the necessary signal processing tools were not well-established, the current work involved the development of new solutions to address the specific requirements of mobile EEG data before real-world brain recordings could be validly interpreted. In a series of Event Related Potential (ERP) experiments, real-world conditions were compared to traditional lab-based conditions. The neural marker of attention (P300 ERP) was recorded when participants performed an attentional task while walking through the university’s corridors versus standing in the lab. Differences in the classic P300 ERP effect show that attentional processes in the real-world are not the same as those recorded in the lab. Following up on this finding, the attenuation of the P300 effect under real-world conditions was shown to be driven by cognitive demands related to displacement through space rather than the act of walking itself. This is a demonstration, at a brain level, that when walking in the real-world, cognitive resources are reallocated to the processing of visual flow and vestibular information associated with displacement. The findings reflect the dynamic interplay between mind, body, and environment, providing innovative evidence strengthening the embodied framework of human cognition. The same dynamic interplay between body, environment and cognitive function is uniquely represented in real-world navigation. The literature on spatial navigation in humans, however, mainly involved navigating virtual reality environments often while lying on a scanner bed. Most of the evidence on the neural markers of spatial navigation comes from intracranially recorded brain oscillations in rodents. The innovation in this thesis was to investigate brain oscillations associated with cognitive function underlying real-world navigation in humans using surface electrodes. The present work demonstrates that human brain dynamics related to navigational cognitive processes can be recorded in active exploration of real-world environments. The key finding resulting from this novel approach is that real-world spatial navigation is associated with specific neural signatures underlying distinct cognitive functions. Frontal low-frequency oscillations were found to be associated with wayfinding, while parietal high-frequency oscillations were associated with spatial memory. Furthermore, these neural correlates were found to be dynamically modulated depending on the body’s contextual positioning within the environment. Therefore, these findings again provide evidence in support of the embodiment theory of cognition. The final study addressed the concern that findings might reflect walking speed variation. The existing animal literature has shown that low-frequency bands are modulated by walking speed. This study characterised the specific modulations in spectral power as a function of walking speed in humans. Critically the pattern showed no similarity to the spectral patterns found in relation to real-world spatial navigation, confirming the cognitive interpretation of this work. Taken together, these findings provide innovative real-world evidence supporting the theoretical embodiment framework. The neural correlates of attention, memory, and spatial navigation were found to be modulated by the dynamic experience of one’s environment. Beyond this work’s theoretical implications for cognitive sciences, the present findings offer new perspectives for real-world application

Brain Tumour Classification Using Deep Features from Structural MRI

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From locomotion to dance and back : exploring rhythmic sensorimotor synchronization

Le rythme est un aspect important du mouvement et de la perception de l’environnement. Lorsque l’on danse, la pulsation musicale induit une activité neurale oscillatoire qui permet au système nerveux d’anticiper les évènements musicaux à venir. Le système moteur peut alors s’y synchroniser. Cette thèse développe de nouvelles techniques d’investigation des rythmes neuraux non strictement périodiques, tels que ceux qui régulent le tempo naturellement variable de la marche ou la perception rythmes musicaux. Elle étudie des réponses neurales reflétant la discordance entre ce que le système nerveux anticipe et ce qu’il perçoit, et qui sont nécessaire pour adapter la synchronisation de mouvements à un environnement variable. Elle montre aussi comment l’activité neurale évoquée par un rythme musical complexe est renforcée par les mouvements qui y sont synchronisés. Enfin, elle s’intéresse à ces rythmes neuraux chez des patients ayant des troubles de la marche ou de la conscience.Rhythms are central in human behaviours spanning from locomotion to music performance. In dance, self-sustaining and dynamically adapting neural oscillations entrain to the regular auditory inputs that is the musical beat. This entrainment leads to anticipation of forthcoming sensory events, which in turn allows synchronization of movements to the perceived environment. This dissertation develops novel technical approaches to investigate neural rhythms that are not strictly periodic, such as naturally tempo-varying locomotion movements and rhythms of music. It studies neural responses reflecting the discordance between what the nervous system anticipates and the actual timing of events, and that are critical for synchronizing movements to a changing environment. It also shows how the neural activity elicited by a musical rhythm is shaped by how we move. Finally, it investigates such neural rhythms in patient with gait or consciousness disorders

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Can deep brain stimulation of the nucleus basalis of Meynert improve thinking and memory problems in Lewy body dementias?

The Lewy body dementias, Parkinson’s disease dementia and dementia with Lewy bodies, are two of the most common causes of dementia worldwide, and share both a common clinical phenotype and underlying pathology. Despite their growing economic and societal disease burden, there are currently only a small number of limited symptomatic therapies available, while modern approaches to develop disease modifying biologic agents have so far produced little tangible effect. There is growing recognition of the need to explore alternative treatment avenues, and the success of deep brain stimulation (DBS) in modulating aberrant neural network processing to relieve symptoms in other neuropsychiatric diseases raises the possibility that this might be achievable in Lewy body dementias. The nucleus basalis of Meynert (NBM) provides the major source of ascending cholinergic innervation to the cortex, and is proposed to be a key node in multiple distributed cognitive networks. The nucleus degenerates significantly in Lewy body dementias, which correlates closely with the severity of cognitive decline. It is therefore proposed that deep brain stimulation to the NBM may be able to modulate cholinergic transmission to cortex, and thereby impact directly upon dementia symptoms. In this thesis I will present preliminary evidence from two experimental clinical trials of deep brain stimulation to the NBM in Lewy body dementias. I will present data showing that this invasive neurosurgical procedure is both safe and well tolerated in patients with advanced dementia, and that low frequency stimulation may be associated with improvements in both memory functions and neuropsychiatric symptomatology. Furthermore, I will present results from the first direct electrophysiological recordings from human NBM in vivo, showing that activity in the nucleus may reflect levels of sustained attention. Finally, I evaluate the overall clinical impact of this novel therapeutic approach in Lewy body dementias, and discuss how our electrophysiological findings may relate to this, and how they contribute to our existing understanding of the physiological function of NBM