Giulio Bernardi

How skill expertise shapes the brain functional architecture: an fMRI study of visuo-spatial and motor processing in professional racing-car and naive drivers.

The present study was designed to investigate the brain functional architecture that subserves visuo-spatial and motor processing in highly skilled individuals. By using functional magnetic resonance imaging (fMRI), we measured brain activity while eleven Formula racing-car drivers and eleven ‘naïve’ volunteers performed a motor reaction and a visuo-spatial task. Tasks were set at a relatively low level of difficulty such to ensure a similar performance in the two groups and thus avoid any potential confounding effects on brain activity due to discrepancies in task execution. The brain functional organization was analyzed in terms of regional brain response, inter-regional interactions and blood oxygen level dependent (BOLD) signal variability. While performance levels were equal in the two groups, as compared to naïve drivers, professional drivers showed a smaller volume recruitment of task-related regions, stronger connections among task-related areas, and an increased information integration as reflected by a higher signal temporal variability. In conclusion, our results demonstrate that, as compared to naïve subjects, the brain functional architecture sustaining visuo-motor processing in professional racing-car drivers, trained to perform at the highest levels under extremely demanding conditions, undergoes both ‘quantitative’ and ‘qualitative’ modifications that are evident even when the brain is engaged in relatively simple, non-demanding tasks. These results provide novel evidence in favor of an increased ‘neural efficiency’ in the brain of highly skilled individuals.

Increased BOLD Variability in the Parietal Cortex and Enhanced Parieto-Occipital Connectivity during Tactile Perception in Congenitally Blind Individuals

Previous studies in early blind individuals posited a possible role of parieto-occipital connections in conveying nonvisual information to the visual occipital cortex. As a consequence of blindness, parietal areas would thus become able to integrate a greater amount of multimodal information than in sighted individuals. To verify this hypothesis, we compared fMRI-measured BOLD signal temporal variability, an index of efficiency in functional information integration, in congenitally blind and sighted individuals during tactile spatial discrimination and motion perception tasks. In both tasks, the BOLD variability analysis revealed many cortical regions with a significantly greater variability in the blind as compared to sighted individuals, with an overlapping cluster located in the left inferior parietal/anterior intraparietal cortex. A functional connectivity analysis using this region as seed showed stronger correlations in both tasks with occipital areas in the blind as compared to sighted individuals. As BOLD variability reflects neural integration and processing efficiency, these cross-modal plastic changes in the parietal cortex, even if described in a limited sample, reinforce the hypothesis that this region may play an important role in processing nonvisual information in blind subjects and act as a hub in the cortico-cortical pathway from somatosensory cortex to the reorganized occipital areas.

Neural and Behavioral Correlates of Extended Training during Sleep Deprivation in Humans: Evidence for Local, Task-Specific Effects

Recent work has demonstrated that behavioral manipulations targeting specific cortical areas during prolonged wakefulness lead to a region-specific homeostatic increase in theta activity (5–9 Hz), suggesting that theta waves could represent transient neuronal OFF periods (local sleep). In awake rats, the occurrence of an OFF period in a brain area relevant for behavior results in performance errors. Here we investigated the potential relationship between local sleep events and negative behavioral outcomes in humans. Volunteers participated in two prolonged wakefulness experiments (24 h), each including 12 h of practice with either a driving simulation (DS) game or a battery of tasks based on executive functions (EFs). Multiple high-density EEG recordings were obtained during each experiment, both in quiet rest conditions and during execution of two behavioral tests, a response inhibition test and a motor test, aimed at assessing changes in impulse control and visuomotor performance, respectively. In addition, fMRI examinations obtained at 12 h intervals were used to investigate changes in inter-regional connectivity. The EF experiment was associated with a reduced efficiency in impulse control, whereas DS led to a relative impairment in visuomotor control. A specific spatial and temporal correlation was observed between EEG theta waves occurring in task-related areas and deterioration of behavioral performance. The fMRI connectivity analysis indicated that performance impairment might partially depend on a breakdown in connectivity determined by a “network overload.” Present results demonstrate the existence of an association between theta waves during wakefulness and performance errors and may contribute explaining behavioral impairments under conditions of sleep deprivation/restriction.

Evidence of a direct influence between the thalamus and hMT + independent of V1 in the human brain as measured by fMRI

In the present study we employed Conditional Granger Causality (CGC) and Coherence analysis to investigate whether visual motion-related information reaches the human middle temporal complex (hMT+) directly from the Lateral Geniculate Nucleus (LGN) of the thalamus, by-passing the primary visual cortex (V1). Ten healthy human volunteers underwent brain scan examinations by functional magnetic resonance imaging (fMRI) during two optic flow experiments. In addition to the classical LGN-V1-hMT+ pathway, our results showed a significant direct influence of the blood oxygenation level dependent (BOLD) signal recorded in LGN over that in hMT+, not mediated by V1 activity, which strongly supports the existence of a bilateral pathway that connects LGN directly to hMT+ and serves visual motion processing. Furthermore, we evaluated the relative latencies among areas functionally connected in the processing of visual motion. Using LGN as a reference region, hMT+ exhibited a statistically significant earlier peak of activation as compared to V1. In conclusion, our findings suggest the co-existence of an alternative route that directly links LGN to hMT+, bypassing V1. This direct pathway may play a significant functional role for the faster detection of motion and may contribute to explain persistence of unconscious motion detection in individuals with severe destruction of primary visual cortex (blindsight).

It's not all in your car: functional and structural correlates of exceptional driving skills in professional racers

Driving is a complex behavior that requires the integration of multiple cognitive functions. While many studies have investigated brain activity related to driving simulation under distinct conditions, little is known about the brain morphological and functional architecture in professional competitive driving, which requires exceptional motor and navigational skills. Here, 11 professional racing-car drivers and 11 “naïve” volunteers underwent both structural and functional brain magnetic resonance imaging (MRI) scans. Subjects were presented with short movies depicting a Formula One car racing in four different official circuits. Brain activity was assessed in terms of regional response, using an Inter-Subject Correlation (ISC) approach, and regional interactions by mean of functional connectivity. In addition, voxel-based morphometry (VBM) was used to identify specific structural differences between the two groups and potential interactions with functional differences detected by the ISC analysis. Relative to non-experienced drivers, professional drivers showed a more consistent recruitment of motor control and spatial navigation devoted areas, including premotor/motor cortex, striatum, anterior, and posterior cingulate cortex and retrosplenial cortex, precuneus, middle temporal cortex, and parahippocampus. Moreover, some of these brain regions, including the retrosplenial cortex, also had an increased gray matter density in professional car drivers. Furthermore, the retrosplenial cortex, which has been previously associated with the storage of observer-independent spatial maps, revealed a specific correlation with the individual drivers success in official competitions. These findings indicate that the brain functional and structural organization in highly trained racing-car drivers differs from that of subjects with an ordinary driving experience, suggesting that specific anatomo-functional changes may subtend the attainment of exceptional driving performance.

The neural correlates of consciousness in sleep: a no-task, within-state paradigm

What are the neural correlates of consciousness? Studies that have addressed this question in the past either compared neural activity during tasks in which subjects report perceiving a stimulus or not, or have contrasted conscious wakefulness with unconscious sleep or anesthesia. However, such contrasts may include correlates of stimulus processing, response preparation or of changes in behavioral state, rather than of consciousness per se. To overcome these limitations, we developed a no-task, within-state paradigm in which sleeping subjects recorded with high density-EEG reported retrospectively whether they had been conscious or not. We identified specific frontal and parieto-occipital regions showing EEG changes several seconds preceding awakenings that distinguished between reports of consciousness and unconsciousness. While decreased parieto-occipital low-frequency activity was associated with highly perceptual experiences, increased frontal high-frequency activity was associated with highly thought-like experiences. Finally, we identified localized, content-specific activations for faces, spatial setting, movement and speech experienced in dreams.Consciousness never fades during wake. However, if awakened from sleep, sometimes we report dreams and sometimes no experiences. Traditionally, dreaming has been identified with REM sleep, characterized by a wake-like, globally ‘activated’, high-frequency EEG. However, dreaming also occurs in NREM sleep, characterized by prominent low-frequency activity. This challenges our understanding of the neural correlates of conscious experiences in sleep. Using high-density EEG, we contrasted the presence and absence of dreaming within NREM and REM sleep. In both NREM and REM sleep, the presence of dreaming was associated with a local decrease in low-frequency activity in posterior cortical regions. High-frequency activity within these regions correlated with specific dream contents. Monitoring this posterior ‘hot zone’ predicted the presence/absence of dreaming during NREM sleep in real time, suggesting that it may constitute a core correlate of conscious experiences in sleep.

Sleep reverts changes in human gray and white matter caused by wake-dependent training

Learning leads to rapid microstructural changes in gray (GM) and white (WM) matter. Do these changes continue to accumulate if task training continues, and can they be reverted by sleep? We addressed these questions by combining structural and diffusion weighted MRI and high-density EEG in 16 subjects studied during the physiological sleep/wake cycle, after 12 h and 24 h of intense practice in two different tasks, and after post-training sleep. Compared to baseline wake, 12 h of training led to a decline in cortical mean diffusivity. The decrease became even more significant after 24 h of task practice combined with sleep deprivation. Prolonged practice also resulted in decreased ventricular volume and increased GM and WM subcortical volumes. All changes reverted after recovery sleep. Moreover, these structural alterations predicted cognitive performance at the individual level, suggesting that sleeps ability to counteract performance deficits is linked to its effects on the brain microstructure. The cellular mechanisms that account for the structural effects of sleep are unknown, but they may be linked to its role in promoting the production of cerebrospinal fluid and the decrease in synapse size and strength, as well as to its recently discovered ability to enhance the extracellular space and the clearance of brain metabolites.

A topographical organization for action representation in the human brain

How the human brain represents distinct motor features into a unique finalized action still remains undefined. Previous models proposed the distinct features of a motor act to be hierarchically organized in separated, but functionally interconnected, cortical areas. Here, we hypothesized that distinct patterns across a wide expanse of cortex may actually subserve a topographically organized coding of different categories of actions that represents, at a higher cognitive level and independently from the distinct motor features, the action and its final aim as a whole. Using functional magnetic resonance imaging and pattern classification approaches on the neural responses of 14 right‐handed individuals passively watching short movies of hand‐performed tool‐mediated, transitive, and meaningful intransitive actions, we were able to discriminate with a high accuracy and characterize the category‐specific response patterns. Actions are distinctively coded in distributed and overlapping neural responses within an action‐selective network, comprising frontal, parietal, lateral occipital and ventrotemporal regions. This functional organization, that we named action topography, subserves a higher‐level and more abstract representation of finalized actions and has the capacity to provide unique representations for multiple categories of actions. Hum Brain Mapp 36:3832–3844, 2015.

How do children fall asleep? A high-density EEG study of slow waves in the transition from wake to sleep.

Introduction Slow waves, the hallmarks of non‐rapid eye‐movement (NREM) sleep, are thought to reflect maturational changes that occur in the cerebral cortex throughout childhood and adolescence. Recent work in adults has revealed evidence for two distinct synchronization processes involved in the generation of slow waves, which sequentially come into play in the transition to sleep. In order to understand how these two processes are affected by developmental changes, we compared slow waves between children and young adults in the falling asleep period. Methods The sleep onset period (starting 30s before end of alpha activity and ending at the first slow wave sequence) was extracted from 72 sleep onset high‐density EEG recordings (128 electrodes) of 49 healthy subjects (age 8–25). Using an automatic slow wave detection algorithm, the number, amplitude and slope of slow waves were analyzed and compared between children (age 8–11) and young adults (age 20–25). Results Slow wave number and amplitude increased linearly in the falling asleep period in children, while in young adults, isolated high‐amplitude slow waves (type I) dominated initially and numerous smaller slow waves (type II) with progressively increasing amplitude occurred later. Compared to young adults, children displayed faster increases in slow wave amplitude and number across the falling asleep period in central and posterior brain regions, respectively, and also showed larger slow waves during wakefulness immediately prior to sleep. Conclusions Children do not display the two temporally dissociated slow wave synchronization processes in the falling asleep period observed in adults, suggesting that maturational factors underlie the temporal segregation of these two processes. Our findings provide novel perspectives for studying how sleep‐related behaviors and dreaming differ between children and adults. HighlightsIn children slow wave number and amplitude increase in parallel in the transition to sleep.In adults slow wave number and amplitude follow dissociated and intersecting courses.Children show larger and more numerous slow waves in central and posterior brain regions.The younger the child, the faster slow wave amplitude and density increase at sleep onset.Children have larger slow waves during wakefulness immediately prior to sleep.

Local and Widespread Slow Waves in Stable NREM Sleep: Evidence for Distinct Regulation Mechanisms

Previous work showed that two types of slow waves are temporally dissociated during the transition to sleep: widespread, large and steep slow waves predominate early in the falling asleep period (type I), while smaller, more circumscribed slow waves become more prevalent later (type II). Here, we studied the possible occurrence of these two types of slow waves in stable non-REM (NREM) sleep and explored potential differences in their regulation. A heuristic approach based on slow wave synchronization efficiency was developed and applied to high-density electroencephalographic (EEG) recordings collected during consolidated NREM sleep to identify the potential type I and type II slow waves. Slow waves with characteristics compatible with those previously described for type I and type II were identified in stable NREM sleep. Importantly, these slow waves underwent opposite changes across the night, with only type II slow waves displaying a clear homeostatic regulation. In addition, we showed that the occurrence of type I slow waves was often followed by larger type II slow waves, whereas the occurrence of type II slow waves was usually followed by smaller type I waves. Finally, type II slow waves were associated with a relative increase in spindle activity, while type I slow waves triggered periods of high-frequency activity. Our results provide evidence for the existence of two distinct slow wave synchronization processes that underlie two different types of slow waves. These slow waves may have different functional roles and mark partially distinct “micro-states” of the sleeping brain.