Decoding the neural dynamics of free choice in humans.

How do we choose a particular action among equally valid alternatives? Nonhuman primate findings have shown that decision-making implicates modulations in unit firing rates and local field potentials (LFPs) across frontal and parietal cortices. Yet the electrophysiological brain mechanisms that underlie free choice in humans remain ill defined. Here, we address this question using rare intracerebral electroencephalography (EEG) recordings in surgical epilepsy patients performing a delayed oculomotor decision task. We find that the temporal dynamics of high-gamma (HG, 60-140 Hz) neural activity in distinct frontal and parietal brain areas robustly discriminate free choice from instructed saccade planning at the level of single trials. Classification analysis was applied to the LFP signals to isolate decision-related activity from sensory and motor planning processes. Compared with instructed saccades, free-choice trials exhibited delayed and longer-lasting HG activity during the delay period. The temporal dynamics of the decision-specific sustained HG activity indexed the unfolding of a deliberation process, rather than memory maintenance. Taken together, these findings provide the first direct electrophysiological evidence in humans for the role of sustained high-frequency neural activation in frontoparietal cortex in mediating the intrinsically driven process of freely choosing among competing behavioral alternatives.

Dissociation between dreams and wakefulness: Insights from body and action representations of rare individuals with massive somatosensory deafferentation.

The realism of body and actions in dreams is thought to be induced by simulations based on internal representations used during wakefulness. As somatosensory signals contribute to the updating of body and action representations, these are impaired when somatosensory signals are lacking. Here, we tested the hypothesis that individuals with somatosensory deafferentation have impaired body and actions in their dreams, as in wakefulness. We questioned three individuals with a severe, acquired sensory neuropathy on their dreams. While deafferented participants were impaired in daily life, they could dream of themselves as able-bodied, with some sensations (touch, proprioception) and actions (such as running or jumping) which had not been experienced in physical life since deafferentation. We speculate that simulation in dreams could be based on former, "healthy" body and action representations. Our findings are consistent with the idea that distinct body and action representations may be used during dreams and wakefulness.

Rat Retrosplenial Cortical Involvement in Wayfinding Using Visual and Locomotor Cues.

The retrosplenial cortex (RSC) has been implicated in wayfinding using different sensory cues. However, the neural mechanisms of how the RSC constructs spatial representations to code an appropriate route under different sensory cues are unknown. In this study, rat RSC neurons were recorded while rats ran on a treadmill affixed to a motion stage that was displaced along a figure-8-shaped track. The activity of some RSC neurons increased during specific directional displacements, while the activity of other neurons correlated with the running speed on the treadmill regardless of the displacement directions. Elimination of visual cues by turning off the room lights and/or locomotor cues by turning off the treadmill decreased the activity of both groups of neurons. The ensemble activity of the former group of neurons discriminated displacements along the common central path of different routes in the track, even when visual or locomotor cues were eliminated where different spatial representations must be created based on different sensory cues. The present results provide neurophysiological evidence of an RSC involvement in wayfinding under different spatial representations with different sensory cues.

Does the Cerebellum Implement or Select Geometries? A Speculative Note.

During evolution, living systems, actively interacting with their environment, developed the ability, through sensorimotor contingencies, to construct functional spaces shaping their perception and their movements. These geometries were modularly embedded in specific functional neuro-architectures. In particular, human movements were shown to obey several empirical laws, such as the 2/3 power law, isochrony, or jerk minimization principles, which constrain and adapt motor planning and execution. Outstandingly, such laws can be deduced from a combination of Euclidean, affine, and equi-affine geometries, whose neural correlates have been partly detected in several brain areas including the cerebellum and the basal ganglia. Reviving Pellionisz and Llinas general hypothesis regarding the cerebrum and the cerebellum as geometric machines, we speculate that the cerebellum should be involved in implementing and/or selecting task-specific geometries for motor and cognitive skills. More precisely, the cerebellum is assumed to compute forward internal models to help specific cortical and subcortical regions to select appropriate geometries among, at least, Euclidean and affine geometries. We emphasize that the geometrical role of the cerebellum deserves a renewal of interest, which may provide a better understanding of its specific contributions to motor and associative (cognitive) functions.

Correction to: Victor Semeonovich Gurfnkel (April 2, 1922-January 14, 2020).

In the original publication of the article.

Role of the human retrosplenial cortex/parieto-occipital sulcus in perspective priming.

The ability to imagine the world from a different viewpoint is a fundamental competence for spatial reorientation and for imagining what another individual sees in the environment. Here, we investigated the neural bases of such an ability using functional magnetic resonance imaging. Healthy participants detected target displacements across consecutive views of a familiar virtual room, either from the perspective of an avatar (primed condition) or in the absence of such a prime (unprimed condition). In the primed condition, the perspective at test always corresponded to the avatar's perspective, while in the unprimed condition it was randomly chosen as 0, 45 or 135deg of viewpoint rotation. We observed a behavioral advantage in performing a perspective transformation during the primed condition as compared to an equivalent amount of unprimed perspective change. Although many cortical regions (dorsal parietal, parieto-temporo-occipital junction, precuneus and retrosplenial cortex/parieto-occipital sulcus or RSC/POS) were involved in encoding and retrieving target location from different perspectives and were modulated by the amount of viewpoint rotation, the RSC/POS was the only area showing decreased activity in the primed as compared to the unprimed condition, suggesting that this region anticipates the upcoming perspective change. The retrosplenial cortex/parieto-occipital sulcus appears to play a special role in the allocentric coding of heading directions.

Anticipatory control and spatial cognition in locomotion and navigation through typical development and in cerebral palsy.

Behavioural evidence, summarized in this narrative review, supports a developmental model of locomotor control based on increasing neural integration of spatial reference frames. Two consistent adult locomotor behaviours are head stabilization and head anticipation: the head is stabilized to gravity and leads walking direction. This cephalocaudal orienting organization aligns gaze and vestibula with a reference frame centred on the upcoming walking direction, allowing anticipatory control on body kinematics, but is not fully developed until adolescence. Walking trajectories and those of hand movements share many aspects, including power laws coupling velocity to curvature, and minimized spatial variability. In fact, the adult brain can code trajectory geometry in an allocentric reference frame, irrespective of the end effector, regulating body kinematics thereafter. Locomotor trajectory formation, like head anticipation, matures in early adolescence, indicating common neurocomputational substrates. These late-developing control mechanisms can be distinguished from biomechanical problems in children with cerebral palsy (CP). Children's performance on a novel navigation test, the Magic Carpet, indicates that typical navigation development consists of the increasing integration of egocentric and allocentric reference frames. In CP, right-brain impairment seems to reduce navigation performance due to a maladaptive left-brain sequential egocentric strategy. Spatial integration should be considered more in rehabilitation.

Interaction Between Hippocampus and Cerebellum Crus I in Sequence-Based but not Place-Based Navigation.

To examine the cerebellar contribution to human spatial navigation we used functional magnetic resonance imaging and virtual reality. Our findings show that the sensory-motor requirements of navigation induce activity in cerebellar lobules and cortical areas known to be involved in the motor loop and vestibular processing. By contrast, cognitive aspects of navigation mainly induce activity in a different cerebellar lobule (VIIA Crus I). Our results demonstrate a functional link between cerebellum and hippocampus in humans and identify specific functional circuits linking lobule VIIA Crus I of the cerebellum to medial parietal, medial prefrontal, and hippocampal cortices in nonmotor aspects of navigation. They further suggest that Crus I belongs to 2 nonmotor loops, involved in different strategies: place-based navigation is supported by coherent activity between left cerebellar lobule VIIA Crus I and medial parietal cortex along with right hippocampus activity, while sequence-based navigation is supported by coherent activity between right lobule VIIA Crus I, medial prefrontal cortex, and left hippocampus. These results highlight the prominent role of the human cerebellum in both motor and cognitive aspects of navigation, and specify the cortico-cerebellar circuits by which it acts depending on the requirements of the task.

Taking a Third-Person Perspective Requires Inhibitory Control: Evidence From a Developmental Negative Priming Study.

To determine whether the growing ability to take a third-person perspective (3PP) is explained in part by the growing ability to inhibit a first-person perspective (1PP), 10-year-old children (n = 49) and 22-year-old adults (n = 52) performed a negative priming adaptation of the own body transformation task. Both children and adults were less efficient in adopting a 1PP after they adopted a 3PP-with a smaller amplitude of the negative priming effect with older age-and adults' and children's performances in the own body transformation task were predicted in part by their Stroop interference scores. These results suggest that the growing efficiency to adopt a 3PP is rooted in part in the growing efficiency to inhibit the 1PP.

Increased functional connectivity between superior colliculus and brain regions implicated in bodily self-consciousness during the rubber hand illusion.

Bodily self-consciousness refers to bodily processes operating at personal, peripersonal, and extrapersonal spatial dimensions. Although the neural underpinnings of representations of personal and peripersonal space associated with bodily self-consciousness were thoroughly investigated, relatively few is known about the neural underpinnings of representations of extrapersonal space relevant for bodily self-consciousness. In the search to unravel brain structures generating a representation of the extrapersonal space relevant for bodily self-consciousness, we developed a functional magnetic resonance imaging (fMRI) study to investigate the implication of the superior colliculus (SC) in bodily illusions, and more specifically in the rubber hand illusion (RHi), which constitutes an established paradigm to study the neural underpinnings of bodily self-consciousness. We observed activation of the colliculus ipsilateral to the manipulated hand associated with eliciting of RHi. A generalized form of context-dependent psychophysiological interaction analysis unravelled increased illusion-dependent functional connectivity between the SC and some of the main brain areas previously involved in bodily self-consciousness: right temporoparietal junction (rTPJ), bilateral ventral premotor cortex (vPM), and bilateral postcentral gyrus. We hypothesize that the collicular map of the extrapersonal space interacts with maps of the peripersonal and personal space generated at rTPJ, vPM and the postcentral gyrus, producing a unified representation of space that is relevant for bodily self-consciousness. We suggest that processes of multisensory integration of bodily-related sensory inputs located in this unified representation of space constitute one main factor underpinning emergence of bodily self-consciousness.

Visuospatial transformations and personality: evidence of a relationship between visuospatial perspective taking and self-reported emotional empathy.

In the visuospatial domain, perspective taking is the ability to imagine how a visual scene appears from an external observer's viewpoint, and can be studied by asking subjects to encode object locations in a visual scene where another individual is present and then detecting their displacement when seeing the scene from the other's viewpoint. In the current study, we explored the relationship between visuospatial perspective taking and self-report measures of the cognitive and emotional components of empathy in young adults. To this aim, we employed a priming paradigm, in which the presence of an avatar allowed to anticipate the next perceived perspective on the visual scene. We found that the emotional dimension of empathy was positively correlated with the behavioral advantage provided by the presence of the avatar, relative to unprimed perspective changes. These data suggest a link between the tendency to vicariously experience the others' emotions and the ability to perform self-other spatial transformations.

Switching from reaching to navigation: differential cognitive strategies for spatial memory in children and adults.

Navigational and reaching spaces are known to involve different cognitive strategies and brain networks, whose development in humans is still debated. In fact, high-level spatial processing, including allocentric location encoding, is already available to very young children, but navigational strategies are not mature until late childhood. The Magic Carpet (MC) is a new electronic device translating the traditional Corsi Block-tapping Test (CBT) to navigational space. In this study, the MC and the CBT were used to assess spatial memory for navigation and for reaching, respectively. Our hypothesis was that school-age children would not treat MC stimuli as navigational paths, assimilating them to reaching sequences. Ninety-one healthy children aged 6 to 11 years and 18 adults were enrolled. Overall short-term memory performance (span) on both tests, effects of sequence geometry, and error patterns according to a new classification were studied. Span increased with age on both tests, but relatively more in navigational than in reaching space, particularly in males. Sequence geometry specifically influenced navigation, not reaching. The number of body rotations along the path affected MC performance in children more than in adults, and in women more than in men. Error patterns indicated that navigational sequences were increasingly retained as global paths across development, in contrast to separately stored reaching locations. A sequence of spatial locations can be coded as a navigational path only if a cognitive switch from a reaching mode to a navigation mode occurs. This implies the integration of egocentric and allocentric reference frames, of visual and idiothetic cues, and access to long-term memory. This switch is not yet fulfilled at school age due to immature executive functions.

Crista egregia: a geometrical model of the crista ampullaris, a sensory surface that detects head rotations.

The crista ampullaris is the epithelium at the end of the semicircular canals in the inner ear of vertebrates, which contains the sensory cells involved in the transduction of the rotational head movements into neuronal activity. The crista surface has the form of a saddle, or a pair of saddles separated by a crux, depending on the species and the canal considered. In birds, it was described as a catenoid by Landolt et al. (J Comp Neurol 159(2):257-287, doi: 10.1002/cne.901590207 , 1972). In the present work, we establish that this particular form results from principles of invariance maximization and energy minimization. The formulation of the invariance principle was inspired by Takumida (Biol Sci Space 15(4):356-358, 2001). More precisely, we suppose that in functional conditions, the equations of linear elasticity are valid, and we assume that in a certain domain of the cupula, in proximity of the crista surface, (1) the stress tensor of the deformed cupula is invariant under the gradient of the pressure, (2) the dissipation of energy is minimum. Then, we deduce that in this domain the crista surface is a minimal surface and that it must be either a planar, or helicoidal Scherk surface, or a piece of catenoid, which is the unique minimal surface of revolution. If we add the hypothesis that the direction of invariance of the stress tensor is unique and that a bilateral symmetry of the crista exists, only the catenoid subsists. This finding has important consequences for further functional modeling of the role of the vestibular system in head motion detection and spatial orientation.

New paradigms and tests for evaluating and remediating visuospatial deficits in children.

This review suggests several hypotheses about the cognitive developmental mechanisms involved in the motor deficits of children with cerebral palsy. We suggest a new theory that visuospatial deficits involving the manipulation of multiple spatial reference frames are crucial components of the disorder in spatial orientation, manipulation, locomotion, navigation, and even social interactions. We review basic knowledge about the brain networks involved in spatial memory and cognition. We then present several potential paradigms for studying specific deficits. We consider first the use of vestibular signals for egocentric spatial orientation in children and the 'locomotor trajectory paradigm' for studying gaze anticipation and perceptual components of walking. We then describe new paradigms for studying egocentric and allocentric strategies in spatial tasks: the 'virtual path length', the 'virtual palace' and the 'virtual star maze'. We also consider paradigms involving the use of other persons and perspective change from a first person's to a third person's viewpoint as reference in spatial tasks or social interactions: the 'designation' paradigm, the 'harlequin', and the 'tightrope walker'. Finally, we briefly present a new experimental set up involving a 'virtual carpet', which follows previous studies of cognitive strategies for generating locomotor trajectories using the 'magic carpet' and which will allow a large variety of studies involving executive functions and inhibition of the first-appearing strategies during development. Several of these new paradigms could be used for remediation.

Cognitive strategies for locomotor navigation in normal development and cerebral palsy.

Visual-spatial impairment is a fundamental disorder in cerebral palsy (CP). However, current spatial testing is restricted to reaching space, whereas navigational space is seldom assessed. The Magic Carpet test, derived from the Corsi Block-tapping Task (CBT) for visual-spatial memory, is a new developmental test for navigation. The performances of the Magic Carpet test and CBT were assessed in 17 children with unilateral and bilateral spastic CP. The results were compared with an equal number of typically developing children, matched for age and sex. Magnetic resonance imaging scans of children with CP were scored according to a newly validated semi-quantitative classification. CBT span was significantly lower in CP, especially in bilateral forms, than in the comparison group, whereas the Magic Carpet test span did not significantly differ between the groups. CBT span, but not the Magic Carpet span, was related to gestational age at birth and to basic visual function. Both the CBT span and the Magic Carpet test were related to overall right-hemispheric impairment. In addition, CBT correlated with right periventricular impairment. In CP, navigation is differently impaired than visual spatial memory, and less tightly related to preterm birth, basic visual function, and deep white matter injury. The exploration of navigational space could prove useful in enhancing spatial representation and reference-frame manipulation in CP.

Disturbances of spontaneous empathic processing relate with the severity of the negative symptoms in patients with schizophrenia: a behavioural pilot-study using virtual reality technology.

Behavioural and neuroimaging data have recently pointed out that empathy (feeling into someone else) is associated with mental imagery and transformation related to one's and other's visuo-spatial perspectives. Impairments of both empathic and visuo-spatial abilities have been observed in patients with schizophrenia. Especially, it has been suggested that schizophrenics are altered in spontaneously simulating another individual's first-person experience. However, there is so far only little evidence regarding the relationship between deficits in empathy and disturbances in spontaneous heterocentered coding in schizophrenia. In the present pilot-study, we tested with schizophrenic patients our behavioural paradigm that enables to measure from the bodily postures and movements whether individuals in ecologically more valid conditions are interacting with another individual by using egocentered - as in sympathy (feeling with someone else) - or heterocentered - as in empathy - visuo-spatial mechanisms. For that, ten patients and ten controls, standing and moving, interacted with a virtual tightrope walker, displayed life-sized, standing and moving as well. We show that patients with higher negative symptoms had, in most cases, deficits in spontaneously using heterocentered visuo-spatial mechanisms and employed preferentially an egocentered referencing to interact with the avatar. In contrast, preserved spontaneous heterocentered visuo-spatial strategies were not linked to a prevailing negative or positive symptomatology. Our data suggest that the severity of the negative symptoms in schizophrenia relates with disturbances of spontaneous ("on-line") empathic processing in association with lower scoring self-reported trait cognitive empathy.

When up is down in 0g: how gravity sensing affects the timing of interceptive actions.

Humans are known to regulate the timing of interceptive actions by modeling, in a simplified way, Newtonian mechanics. Specifically, when intercepting an approaching ball, humans trigger their movements a bit earlier when the target arrives from above than from below. This bias occurs regardless of the ball's true kinetics, and thus appears to reflect an a priori expectation that a downward moving object will accelerate. We postulate that gravito-inertial information is used to tune visuomotor responses to match the target's most likely acceleration. Here we used the peculiar conditions of parabolic flight--where gravity's effects change every 20 s--to test this hypothesis. We found a striking reversal in the timing of interceptive responses performed in weightlessness compared with trials performed on ground, indicating a role of gravity sensing in the tuning of this response. Parallels between these observations and the properties of otolith receptors suggest that vestibular signals themselves might plausibly provide the critical input. Thus, in addition to its acknowledged importance for postural control, gaze stabilization, and spatial navigation, we propose that detecting the direction of gravity's pull plays a role in coordinating quick reactions intended to intercept a fast-moving visual target.

Long-distance amplitude correlations in the high γ band reveal segregation and integration within the reading network.

Reading sentences involves a distributed network of brain regions acting in concert surrounding the left sylvian fissure. The mechanisms of neural communication underlying the extraction and integration of verbal information across subcomponents of this reading network are still largely unknown. We recorded intracranial EEG activity in 12 epileptic human patients performing natural sentence reading and analyzed long-range corticocortical interactions between local neural activations. During a simple task contrasting semantic, phonological, and purely visual processes, we found process-specific neural activity elicited at the single-trial level, characterized by energy increases in a broad gamma band (40-150 Hz). Correlation analysis between task-induced gamma-band activations revealed a selective fragmentation of the network into specialized subnetworks supporting sentence-level semantic analysis and phonological processing. We extend the implications of our results beyond reading, to propose that gamma-band amplitude correlations might constitute a fundamental mechanism for large-scale neural integration during high-level cognition.

Timing of posterior parahippocampal gyrus activity reveals multiple scene processing stages.

Posterior parahippocampal gyrus (PPHG) is strongly involved during scene recognition and spatial cognition. How PPHG electrophysiological activity could underlie these functions, and whether they share similar timing mechanisms is unknown. We addressed this question in two intracerebral experiments which revealed that PPHG neural activity dissociated an early stimulus-driven effect (>200 and <500 ms) and a late task-related effect (>600 and <800 ms). Strongest PPHG gamma band (50-150 Hz) activities were found early when subjects passively viewed scenes (scene selectivity effect) and lately when they had to estimate the position of an object relative to the environment (allocentric effect). Based on single trial analyses, we were able to predict when patients viewed scenes (compared to other visual categories) and when they performed allocentric judgments (compared to other spatial judgments). The anatomical location corresponding to the strongest effects was in the depth of the collateral sulcus. Our findings directly affect current theories of visual scene processing and spatial orientation by providing new timing constraints and by demonstrating the existence of separable information processing stages in the functionally defined parahippocampal place area.

Striola magica. A functional explanation of otolith geometry.

Otolith end organs of vertebrates sense linear accelerations of the head and gravitation. The hair cells on their epithelia are responsible for transduction. In mammals, the striola, parallel to the line where hair cells reverse their polarization, is a narrow region centered on a curve with curvature and torsion. It has been shown that the striolar region is functionally different from the rest, being involved in a phasic vestibular pathway. We propose a mathematical and computational model that explains the necessity of this amazing geometry for the striola to be able to carry out its function. Our hypothesis, related to the biophysics of the hair cells and to the physiology of their afferent neurons, is that striolar afferents collect information from several type I hair cells to detect the jerk in a large domain of acceleration directions. This predicts a mean number of two calyces for afferent neurons, as measured in rodents. The domain of acceleration directions sensed by our striolar model is compatible with the experimental results obtained on monkeys considering all afferents. Therefore, the main result of our study is that phasic and tonic vestibular afferents cover the same geometrical fields, but at different dynamical and frequency domains.