Medial positioning of the hippocampus and hippocampal fissure volume in developmental topographical disorientation.

Developmental topographical disorientation (DTD) refers to the lifelong inability to orient by means of cognitive maps in familiar surroundings despite otherwise well-preserved general cognitive functions, and the absence of any acquired brain injury or neurological condition. While reduced functional connectivity between the hippocampus and other brain regions has been reported in DTD individuals, no structural differences in gray matter tissue for the whole brain neither for the hippocampus were detected. Considering that the human hippocampus is the main structure associated with cognitive map-based navigation, here, we investigated differences in morphological and morphometric hippocampal features between individuals affected by DTD (N = 20) and healthy controls (N = 238). Specifically, we focused on a developmental anomaly of the hippocampus that is characterized by the incomplete infolding of hippocampal subfields during fetal development, giving the hippocampus a more round or pyramidal shape, called incomplete hippocampal inversion (IHI). We rated IHI according to standard criteria and extracted hippocampal subfield volumes after FreeSurfer's automatic segmentation. We observed similar IHI prevalence in the group of individuals with DTD with respect to the control population. Neither differences in whole hippocampal nor major hippocampal subfield volumes have been observed between groups. However, when assessing the IHI independent criteria, we observed that the hippocampus in the DTD group is more medially positioned comparing to the control group. In addition, we observed bigger hippocampal fissure volume for the DTD comparing to the control group. Both of these findings were stronger for the right hippocampus comparing to the left. Our results provide new insights regarding the hippocampal morphology of individuals affected by DTD, highlighting the role of structural anomalies during early prenatal development in line with the developmental nature of the spatial disorientation deficit.

Foot-related/walking macro-affordances are implicitly activated and preferentially guided by the framing distance of the environmental layout.

As classically captured in the notion of affordance, the natural environment presents animals with multiple opportunities for action and locomotion appears as the privileged form of action to cover distance in the extrapersonal space/environment. We have recently described a facilitation effect, known as "macro-affordance", for the execution of walking-related actions in response to distant vs. near objects/locations in the extrapersonal space. However, since the manipulation of distance was coextensive to landmark-objects contained in the environment and to the environmental layout per se, the relative contribution of these two factors remains undetermined. In addition, since the effect was originally described in the context of an incidental priming paradigm, it is still unknown whether it was specifically associated with an implicit coding of environmental distance. Here, across three experiments, we examined the degree to which the "macro-affordance" effect reflects (i) the encoding of environmental vs. landmark-objects' distance, (ii) the involvement of an implicit vs. controlled system, (iii) a foot-effector specificity. The results showed that the "macro-affordance" effect is more efficiently triggered by the framing distance of the environmental layout (far/wide/panoramic vs. near/close/restricted) rather than of isolated landmark-objects in the environment and that it only emerges when the distance dimension is implicitly processed within the incidental priming paradigm. The results additionally suggested a specificity of the effect for foot- vs. hand-related actions. The present findings suggest that macro-affordances reflect an implicit coding of spatial features of the environmental layout and viewer-environment relationships that preferentially guide a walking-related exploration of the spatial environment.

Empowering episodic memory through a model-based egocentric navigational training.

Recent works have proposed that spatial mechanisms in the hippocampal-entorhinal system might have originally developed to represent distances and positions in the physical space and successively evolved to represent experience and memory in the mental space (Bellmund et al. 2018; Bottini and Doeller 2020). Within this phylogenetic continuity hypothesis (Buzsáki and Moser 2013), mechanisms supporting episodic and semantic memory would have evolved from egocentric and allocentric spatial navigation mechanisms, respectively. Recent studies have described a specific relationship between human performance in egocentric navigation and episodic memory (Committeri et al. 2020; Fragueiro et al. 2021), representing the first behavioral support to this hypothesis. Here, we tested the causal relationship among egocentric navigation and both episodic and semantic components of declarative memory. We conducted two experiments on healthy young adults: in the first experiment, participants were submitted to a navigational training based on path integration, while in the second experiment, participants completed a control training based on visual-perceptual learning. Performance in a set of memory tasks assessing episodic, semantic and short-term memory was compared among the pre- vs. post-training sessions. The results indicated a significant improvement of the episodic memory but not of the semantic or the short-term memory performance following the navigational training. In addition, no modulations of performance across the three memory tasks were observed following the control perceptual training. Our findings provide brand-new evidence of a potential causal association between mechanisms of egocentric navigation and episodic memory, thereby further supporting the phylogenetic continuity hypothesis between navigation and memory mechanisms as well as offering new insights about possible clinical applications of navigational trainings for memory functions/dysfunctions.

Selective effects of a brain tumor on the metric representation of the hand: a pre- versus post-surgery comparison.

Body representation disorders are complex, varied, striking, and very disabling in most cases. Deficits of body representation have been described after lesions to multimodal and sensorimotor cortical areas. A few studies have reported the effects of tumors on the representation of the body, but little is known about the changes after tumor resection. Moreover, the impact of brain lesions on the hand size representation has been investigated in few clinical cases. Hands are of special importance, as no other body part has the ability for movement and interaction with the environment that the hands have, and we use them for a multitude of daily activities. Studies with clinical population can add further knowledge into the way hands are represented. Here, we report a single case study of a patient (AM) who was an expert bodybuilder and underwent a surgery to remove a glioblastoma in the left posterior prefrontal and precentral cortex at the level of the hand's motor region. Pre- (20 days) and post- (4 months) surgery assessment did not show any motor or cognitive impairments. A hand localization task was used, before and after surgery (12 months), to measure possible changes of the metric representation of his right hand. Results showed a post-surgery modulation of the typically distorted hand representation, with an overall accuracy improvement, especially on width dimension. These findings support the direct involvement of sensorimotor areas in the implicit representation of the body size and its relevance on defining specific size representation dimensions.

Distinct connectivity profiles predict different in-time processes of motor skill learning.

Learning through intensive practice has been largely observed in motor, sensory and higher-order cognitive processing. Neuroimaging studies have shown that learning phases are associated with different patterns of functional and structural neural plasticity in spatially distributed brain systems. Yet, it is unknown whether distinct neural signatures before practice can foster different subsequent learning stages over time. Here, we employed a bimanual implicit sequence reaction time task (SRTT) to investigate whether the rates of early (one day after practice) and late (one month after practice) post-training motor skill learning were predicted by distinct patterns of pre-training resting state functional connectivity (rs-FC), recorded with functional MRI. We observed that both motor learning descriptors were positively correlated with the strength of rs-FC among pairs of regions within a SRTT-relevant network comprising cerebellar as well as cortical and subcortical motor areas. Crucially, we detected a double dissociation such that early post-training learning was significantly associated with the functional connections within cerebellar regions, whereas late post-training learning was significantly related to the functional connections between cortical and subcortical motor areas. These findings indicate that spontaneous brain activity prospectively carries out behaviorally relevant information to perform experience-dependent cognitive operations far distant in time.

Causal topography of visual cortex in perceptual learning.

Individuals are able to improve their visual skill with practice, a phenomenon called Visual Perceptual Learning (VPL). We previously observed that after training on a difficult shape identification task, the dorsal visual regions (i.e. right V2d/V3 and right lateral occipital, LO) corresponding to the trained visual quadrant, and their homologous in the opposite hemisphere, exhibited a selective activation at the end of the learning. By contrast, such modulation was not observed in the ventral visual regions, corresponding to the untrained quadrants. The causal role of the trained visual cortex was previously showed in a TMS study as its inactivation impaired behavioral performance to learned stimuli. Here, using the same experimental design, we employed TMS over the homologous of the trained area (i.e. left V2d/V3) as well as over the untrained region (i.e. right V4) to causally map the visual network during the perceptual learning. We report a decrease of accuracy after TMS over left V2d/V3 as compared to both right V4 and Sham (inactive stimulation) conditions. Importantly, TMS effect was correlated with the degree of learning, such that subjects with lower accuracy at the end of the training exhibited stronger TMS impairment. These results provide evidence that segregated regions within the visual network are causally involved in visual perceptual learning.

Neural bases of self- and object-motion in a naturalistic vision.

To plan movements toward objects our brain must recognize whether retinal displacement is due to self-motion and/or to object-motion. Here, we aimed to test whether motion areas are able to segregate these types of motion. We combined an event-related functional magnetic resonance imaging experiment, brain mapping techniques, and wide-field stimulation to study the responsivity of motion-sensitive areas to pure and combined self- and object-motion conditions during virtual movies of a train running within a realistic landscape. We observed a selective response in MT to the pure object-motion condition, and in medial (PEc, pCi, CSv, and CMA) and lateral (PIC and LOR) areas to the pure self-motion condition. Some other regions (like V6) responded more to complex visual stimulation where both object- and self-motion were present. Among all, we found that some motion regions (V3A, LOR, MT, V6, and IPSmot) could extract object-motion information from the overall motion, recognizing the real movement of the train even when the images remain still (on the screen), or moved, because of self-movements. We propose that these motion areas might be good candidates for the "flow parsing mechanism," that is the capability to extract object-motion information from retinal motion signals by subtracting out the optic flow components.

The effect of reward expectation on the time course of perceptual decisions.

Perceptual discriminations can be strongly biased by the expected reward for a correct decision but the neural mechanisms underlying this influence are still partially unclear. Using functional magnetic resonance imaging (fMRI) during a task requiring to arbitrarily associate a visual stimulus with a specific action, we have recently shown that perceptual decisions are encoded within the same sensory-motor regions responsible for planning and executing specific motor actions. Here we examined whether these regions additionally encode the amount of expected reward for a perceptual decision. Using a task requiring to associate a gradually unmasked female vs. male picture with a spatially-directed hand pointing or saccadic eye movement, we examined whether the fMRI time course of effector-selective regions was modulated by the amount of expected reward. In both the pointing-selective parietal reach region (PRR) and the saccade-selective posterior intraparietal region (pIPS), reward-related modulations were only observed after the onset of the stimulus, during decision formation. However, while in the PRR these modulations were specific for the preferred pointing response, the pIPS showed greater activity when either a saccadic or a pointing movement was associated with a greater reward relative to neutral conditions. Interestingly, the fusiform face area showed a similar reward-related but response-independent modulation, consistent with a general motivational signal rather than with a mechanism for biasing specific sensory or motor representations. Together, our results support an account of perception as a process of probabilistic inference in which top-down and bottom-up information are integrated at every level of the cortical hierarchy.

Transcranial direct current stimulation (tDCS) of the inferior frontal cortex affects the "social scaling" of extrapersonal space depending on perspective-taking ability.

When we have to judge the distance between another person and an object (social condition), we judge this distance as being smaller compared to judging the distance between two objects (nonsocial condition). It has been suggested that this compression is mediated by the attribution of a motor potential to the reference frame (other person vs. object). In order to explore the neural basis of this effect, we investigated whether the modulation of activity in the inferior frontal cortex (IFC) of the left hemisphere (recruited during visuospatial processes with a social component) changes the way we categorize space in a social compared with a nonsocial condition. We applied transcranial direct current stimulation to the left IFC, with different polarities (anodal, cathodal, and sham) while subjects performed an extrapersonal space categorization task. Interestingly, anodal stimulation of IFC induced an higher compression of space in the social compared to nonsocial condition. By contrast, cathodal stimulation induced the opposite effect. Furthermore, we found that this effect is modulated by interindividual differences in cognitive perspective taking. Our data support the idea that IFC is recruited during the social categorization of space.

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.

Magnetic stimulation of visual cortex impairs perceptual learning.

The ability to learn and process visual stimuli more efficiently is important for survival. Previous neuroimaging studies have shown that perceptual learning on a shape identification task differently modulates activity in both frontal-parietal cortical regions and visual cortex (Sigman et al., 2005;Lewis et al., 2009). Specifically, fronto-parietal regions (i.e. intra parietal sulcus, pIPS) became less activated for trained as compared to untrained stimuli, while visual regions (i.e. V2d/V3 and LO) exhibited higher activation for familiar shape. Here, after the intensive training, we employed transcranial magnetic stimulation over both visual occipital and parietal regions, previously shown to be modulated, to investigate their causal role in learning the shape identification task. We report that interference with V2d/V3 and LO increased reaction times to learned stimuli as compared to pIPS and Sham control condition. Moreover, the impairment observed after stimulation over the two visual regions was positive correlated. These results strongly support the causal role of the visual network in the control of the perceptual learning.

Brain activity modulation during the production of imperative and declarative pointing.

Pointing is a communicative gesture, commonly used for expressing two main intentions: imperative, to obtain a desired object/action from the other, or declarative, to share attention/interest about a referent with the other. Previous neuroimaging research on adults examined pointing almost exclusively as a reaching-like motor act rather than as a communicative gesture. Here, we used fMRI to record brain activity while 16 participants produced either imperative or declarative pointing gestures within a communicative context. A network of regions (the bilateral ventral premotor cortex, anterior midcingulate cortex, middle insula and the right preSMA) showed a preference for the production of declarative pointing as opposed to imperative pointing. The right preSMA also preferred declarative intention during pointing observation. Instead, independently from the intention, the right pMTG was more active during pointing observation than production. In the bilateral posterior parietal reach region we also observed a side (contra>ipsi) effect when the intention was imperative, regardless of the subject's role in the communication. Based on these results, we propose that pointing with declarative intention recruits a network of regions associated with will, motivation, emotional/affective expression and intersubjectivity, whereas pointing with imperative intention recruits regions associated with reaching. The proposal is consistent with the developmental hypothesis that declarative pointing reflects social cognitive abilities more than imperative pointing and establishes a stimulating link for future interdisciplinary research.

Analysis of hand kinematics reveals inter-individual differences in intertemporal decision dynamics.

During intertemporal decisions, the preference for smaller, sooner reward over larger-delayed rewards (temporal discounting, TD) exhibits substantial inter-subject variability; however, it is currently unclear what are the mechanisms underlying this apparently idiosyncratic behavior. To answer this question, here we recorded and analyzed mouse movement kinematics during intertemporal choices in a large sample of participants (N = 86). Results revealed a specific pattern of decision dynamics associated with the selection of "immediate" versus "delayed" response alternatives, which well discriminated between a "discounter" versus a "farsighted" behavior-thus representing a reliable behavioral marker of TD preferences. By fitting the Drift Diffusion Model to the data, we showed that differences between discounter and farsighted subjects could be explained in terms of different model parameterizations, corresponding to the use of different choice mechanisms in the two groups. While farsighted subjects were biased toward the "delayed" option, discounter subjects were not correspondingly biased toward the "immediate" option. Rather, as shown by the dynamics of evidence accumulation over time, their behavior was characterized by high choice uncertainty.

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.

Age-related effects on spatial memory across viewpoint changes relative to different reference frames.

Remembering object positions across different views is a fundamental competence for acting and moving appropriately in a large-scale space. Behavioural and neurological changes in elderly subjects suggest that the spatial representations of the environment might decline compared to young participants. However, no data are available on the use of different reference frames within topographical space in aging. Here we investigated the use of allocentric and egocentric frames in aging, by asking young and older participants to encode the location of a target in a virtual room relative either to stable features of the room (allocentric environment-based frame), or to an unstable objects set (allocentric objects-based frame), or to the viewer's viewpoint (egocentric frame). After a viewpoint change of 0° (absent), 45° (small) or 135° (large), participants judged whether the target was in the same spatial position as before relative to one of the three frames. Results revealed a different susceptibility to viewpoint changes in older than young participants. Importantly, we detected a worst performance, in terms of reaction times, for older than young participants in the allocentric frames. The deficit was more marked for the environment-based frame, for which a lower sensitivity was revealed as well as a worst performance even when no viewpoint change occurred. Our data provide new evidence of a greater vulnerability of the allocentric, in particular environment-based, spatial coding with aging, in line with the retrogenesis theory according to which cognitive changes in aging reverse the sequence of acquisition in mental development.

Individual variability in functional connectivity predicts performance of a perceptual task.

People differ in their ability to perform novel perceptual tasks, both during initial exposure and in the rate of improvement with practice. It is also known that regions of the brain recruited by particular tasks change their activity during learning. Here we investigate neural signals predictive of individual variability in performance. We used resting-state functional MRI to assess functional connectivity before training on a novel visual discrimination task. Subsequent task performance was related to functional connectivity measures within portions of visual cortex and between visual cortex and prefrontal association areas. Our results indicate that individual differences in performing novel perceptual tasks can be related to individual differences in spontaneous cortical activity.

Decision and action planning signals in human posterior parietal cortex during delayed perceptual choices.

During simple perceptual decisions, sensorimotor neurons in monkey fronto-parietal cortex represent a decision variable that guides the transformation of sensory evidence into a motor response, supporting the view that mechanisms for decision-making are closely embedded within sensorimotor structures. Within these structures, however, decision signals can be dissociated from motor signals, thus indicating that sensorimotor neurons can play multiple and independent roles in decision-making and action selection/planning. Here we used functional magnetic resonance imaging to examine whether response-selective human brain areas encode signals for decision-making or action planning during a task requiring an arbitrary association between face pictures (male vs. female) and specific actions (saccadic eye vs. hand pointing movements). The stimuli were gradually unmasked to stretch the time necessary for decision, thus maximising the temporal separation between decision and action planning. Decision-related signals were measured in parietal and motor/premotor regions showing a preference for the planning/execution of saccadic or pointing movements. In a parietal reach region, decision-related signals were specific for the stimulus category associated with its preferred pointing response. By contrast, a saccade-selective posterior intraparietal sulcus region carried decision-related signals even when the task required a pointing response. Consistent signals were observed in the motor/premotor cortex. Whole-brain analyses indicated that, in our task, the most reliable decision signals were found in the same neural regions involved in response selection. However, decision- and action-related signals within these regions can be dissociated. Differences between the parietal reach region and posterior intraparietal sulcus plausibly depend on their functional specificity rather than on the task structure.

Embodied and disembodied allocentric simulation in high schizotypal subjects.

It is known that non-clinical subjects with high levels of schizotypal personality traits (High-S), as well as schizophrenic patients, have difficulties to judge how a scene would appear (so-called Appearance questions) from a point of view other than their own after having performed a disembodied perspective taking (D-PT, a mental self-rotation cued by an object like a chair). This inability has been defined allocentric simulation deficit. However, it is still unclear whether this inability might also regard an embodied transformation (E-PT), which is a self-rotation cued by another individual in the scene, and whether the observed deficit regards the pure mental transformation phase. In the present study, we took advantage of a virtual reality environment to explore both embodied and disembodied allocentric simulation in healthy volunteers with low and high levels of schizotypal personality traits, as assessed by the Schizotypal Personality Questionnaire. All subjects performed a pure self-rotation cued by a chair (D-PT) or by an avatar (E-PT), or a control array rotation. Each rotation was followed by classical Appearance and Item questions. Results revealed no between-groups differences in the mental transformation phase, while High-S subjects were significantly slower than Low-S subjects in the Appearance task after D-PT, but not after E-PT. Accordingly, higher schizotypy levels (cognitive-perceptual subscale) were positively correlated with slower reaction times in the Appearance task after D-PT. These data suggest the existence of a disembodied allocentric simulation deficit in non-clinical High-S, paving the way to future studies on clinical populations.

Unlocking the potential of 'passive' modulation: How sensory stimulation shapes hand and face size.

Knowledge of the body size is intricately tied to multisensory integration processes that rely on the dynamic interplay of top-down and bottom-up mechanisms. Recent years have seen the development of passive sensory stimulation protocols aimed at investigating the modulation of various cognitive functions, primarily inducing perceptual learning and behaviour change without the need for extensive training. Given that reductions in sensory input have been associated with alterations in body size perception, it is reasonable to hypothesize that increasing sensory information through passive sensory stimulation could similarly influence the perception of the size of body parts. The primary aim of this study was to investigate the potential modulatory effects of passive sensory stimulation on the perception of hand and face size in a group of young adults. Passive sensory stimulation effectively modulated the size representation of the stimulated hand, supporting the notion that access to somatosensory and proprioceptive information is prioritised for the hands but may not extend to the face. Increased somatosensory input resulted in a reduction of distortion, providing evidence for bottom-up modulation of size representation. Passive sensory stimulation can induce subjective changes in body size perception without the need for extensive training. This paradigm holds promise as a potential alternative for modulating distorted size representation in individuals with body representational deficits.

Human intraparietal sulcal morphology relates to individual differences in language and memory performance.

The sulco-gyral pattern is a qualitative feature of the cortical anatomy that is determined in utero, stable throughout lifespan and linked to brain function. The intraparietal sulcus (IPS) is a nodal associative brain area, but the relation between its morphology and cognition is largely unknown. By labelling the left and right IPS of 390 healthy participants into two patterns, according to the presence or absence of a sulcus interruption, here we demonstrate a strong association between the morphology of the right IPS and performance on memory and language tasks. We interpret the results as a morphological advantage of a sulcus interruption, probably due to the underlying white matter organization. The right-hemisphere specificity of this effect emphasizes the neurodevelopmental and plastic role of sulcus morphology in cognition prior to lateralisation processes. The results highlight a promising area of investigation on the relationship between cognitive performance, sulco-gyral pattern and white matter bundles.