Neural sensitivity to translational self- and object-motion velocities.

The ability to detect and assess world-relative object-motion is a critical computation performed by the visual system. This computation, however, is greatly complicated by the observer's movements, which generate a global pattern of motion on the observer's retina. How the visual system implements this computation is poorly understood. Since we are potentially able to detect a moving object if its motion differs in velocity (or direction) from the expected optic flow generated by our own motion, here we manipulated the relative motion velocity between the observer and the object within a stationary scene as a strategy to test how the brain accomplishes object-motion detection. Specifically, we tested the neural sensitivity of brain regions that are known to respond to egomotion-compatible visual motion (i.e., egomotion areas: cingulate sulcus visual area, posterior cingulate sulcus area, posterior insular cortex [PIC], V6+, V3A, IPSmot/VIP, and MT+) to a combination of different velocities of visually induced translational self- and object-motion within a virtual scene while participants were instructed to detect object-motion. To this aim, we combined individual surface-based brain mapping, task-evoked activity by functional magnetic resonance imaging, and parametric and representational similarity analyses. We found that all the egomotion regions (except area PIC) responded to all the possible combinations of self- and object-motion and were modulated by the self-motion velocity. Interestingly, we found that, among all the egomotion areas, only MT+, V6+, and V3A were further modulated by object-motion velocities, hence reflecting their possible role in discriminating between distinct velocities of self- and object-motion. We suggest that these egomotion regions may be involved in the complex computation required for detecting scene-relative object-motion during self-motion.

Effect of optic flow on spatial updating: insight from an immersive virtual reality study.

Self-motion information is required to keep track of where we are with respect to our environment (spatial updating). Visual signals such as optic flow are relevant to provide information about self-motion, especially in the absence of vestibular and/or proprioceptive cues generated by physical movement. However, the role of optic flow on spatial updating is still debated. A virtual reality system based on a head-mounted display was used to allow participants to experience a self-motion sensation within a naturalistic environment in the absence of physical movement. We asked participants to keep track of spatial positions of a target during simulated self-motion while manipulating the availability of optic flow coming from the lower part of the environment (ground plane). In each trial, the ground could be a green lawn (optic flow ON) or covered in snow (optic flow OFF). We observed that the lack of optic flow on the ground had a detrimental effect on spatial updating. Furthermore, we explored the interaction between the optic flow availability and different characteristics of self-motion: we observed that increasing self-motion speed had a detrimental effect on spatial updating, especially in the absence of optic flow, while self-motion direction (leftward, forward, rightward) and path (translational and curvilinear) had no statically significant effect. Overall, we demonstrated that, in the absence of some idiothetic cues, the optic flow provided by the ground has a dominant role for the self-motion estimation and, hence, for the ability to update the spatial relationships between one's position and the position of the surrounding objects.

Assessing the effective connectivity of premotor areas during real vs imagined grasping: a DCM-PEB approach.

The parieto-frontal circuit underlying grasping, which requires the serial involvement of the anterior intraparietal area (aIPs) and the ventral premotor cortex (PMv), has been recently extended enlightening the role of the dorsal premotor cortex (PMd). The supplementary motor area (SMA) has been also suggested to encode grip force for grasping actions; furthermore, both PMd and SMA are known to play a crucial role in motor imagery. Here, we aimed at assessing the dynamic couplings between left aIPs, PMv, PMd, SMA and primary motor cortex (M1) by comparing executed and imagined right-hand grasping, using Dynamic Causal Modelling (DCM) and Parametrical Empirical Bayes (PEB) analyses. 24 subjects underwent an fMRI exam (3T) during which they were asked to perform or imagine a grasping movement visually cued by photographs of commonly used objects. We tested whether the two conditions a) exert a modulatory effect on both forward and feedback couplings among our areas of interest, and b) differ in terms of strength and sign of these parameters. Results of the real condition confirmed the serial involvement of aIPs, PMv and M1. PMv also exerted a positive influence on PMd and SMA, but received an inhibitory feedback only from PMd. Our results suggest that a general motor program for grasping is planned by the aIPs-PMv circuit; then, PMd and SMA encode high-level features of the movement. During imagery, the connection strength from aIPs to PMv was weaker and the information flow stopped in PMv; thus, a less complex motor program was planned. Moreover, results suggest that SMA and PMd cooperate to prevent motor execution. In conclusion, the comparison between execution and imagery reveals that during grasping premotor areas dynamically interplay in different ways, depending on task demands.

Multisensory integration in cortical regions responding to locomotion-related visual and somatomotor signals.

During real-world locomotion, in order to be able to move along a path or avoid an obstacle, continuous changes in self-motion direction (i.e. heading) are needed. Control of heading changes during locomotion requires the integration of multiple signals (i.e., visual, somatomotor, vestibular). Recent fMRI studies have shown that both somatomotor areas (human PEc [hPEc], human PE [hPE], primary somatosensory cortex [S-I]) and egomotion visual regions (cingulate sulcus visual area [CSv], posterior cingulate area [pCi], posterior insular cortex [PIC]) respond to either leg movements and egomotion-compatible visual stimulations, suggesting a role in the analysis of both visual attributes of egomotion and somatomotor signals with the aim of guiding locomotion. However, whether these regions are able to integrate egomotion-related visual signals with somatomotor inputs coming from leg movements during heading changes remains an open question. Here we used a combined approach of individual functional localizers and task-evoked activity by fMRI. In thirty subjects we first localized three egomotion areas (CSv, pCi, PIC) and three somatomotor regions (S-I, hPE, hPEc). Then, we tested their responses in a multisensory integration experiment combining visual and somatomotor signals relevant to locomotion in congruent or incongruent trials. We used an fMR-adaptation paradigm to explore the sensitivity to the repeated presentation of these bimodal stimuli in the six regions of interest. Results revealed that hPE, S-I and CSv showed an adaptation effect regardless of congruency, while PIC, pCi and hPEc showed sensitivity to congruency. PIC exhibited a preference for congruent trials compared to incongruent trials. Areas pCi and hPEc exhibited an adaptation effect only for congruent and incongruent trials, respectively. PIC, pCi and hPEc sensitivity to the congruency relationship between visual (locomotion-compatible) cues and (leg-related) somatomotor inputs suggests that these regions are involved in multisensory integration processes, likely in order to guide/adjust leg movements during heading changes.

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.

Prompting future events: Effects of temporal cueing and time on task on brain preparation to action.

Prediction about event timing plays a leading role in organizing and optimizing behavior. We recorded anticipatory brain activities and evaluated whether temporal orienting processes are reflected by the novel prefrontal negative (pN) component, as already shown for the contingent negative variation (CNV). Fourteen young healthy participants underwent EEG and fMRI recordings in separate sessions; they were asked to perform a Go/No-Go task in which temporal orienting was manipulated: the external condition (a visual display indicating the time of stimulus onset) and the internal condition (time information not provided). In both conditions, the source of the pN was localized in the pars opercularis of the iFg; the source of the CNV was localized in the supplementary motor area and cingulate motor area, as expected. Anticipatory activity was also found in the occipital-parietal cortex. Time on task EEG analysis showed a marked learning effect in the internal condition, while the effect was minor in the external condition. In fMRI, the two conditions had a similar pattern; similarities and differences of results obtained with the two techniques are discussed. Overall, data are consistent with the view that the pN reflects a proactive cognitive control, including temporal orienting.

A putative human homologue of the macaque area PEc.

The cortical area PEc is anatomically and functionally well-defined in macaque, but it is unknown whether it has a counterpart in human. Since we know that macaque PEc, but not the nearby posterior regions, hosts a lower limb representation, in an attempt to recognize a possible human PEc we looked for the existence of leg representations in the human parietal cortex using individual cortical surface-based analysis, task-evoked paradigms and resting-state functional connectivity. fMRI images were acquired while thirty-one participants performed long-range leg movements through an in-house MRI-compatible set-up. We revealed the existence of multiple leg representations in the human dorsomedial parietal cortex, here defined as S-I (somatosensory-I), hPE (human PE, in the postcentral sulcus), and hPEc (human PEc, in the anterior precuneus). Among the three "leg" regions, hPEc had a unique functional profile, in that it was the only one responding to both arm and leg movements, to both hand-pointing and foot pointing movements, and to flow field visual stimulation, very similar to macaque area PEc. In addition, hPEc showed functional connections with the somatomotor regions hosting a lower limb representation, again as in macaque area PEc. Therefore, based on similarity in brain position, functional organization, cortical connections, and relationship with the neighboring areas, we propose that this cortical region is the human homologue of macaque area PEc.

Egomotion-related visual areas respond to active leg movements.

Monkey neurophysiology and human neuroimaging studies have demonstrated that passive viewing of optic flow stimuli activates a cortical network of temporal, parietal, insular, and cingulate visual motion regions. Here, we tested whether the human visual motion areas involved in processing optic flow signals simulating self-motion are also activated by active lower limb movements, and hence are likely involved in guiding human locomotion. To this aim, we used a combined approach of task-evoked activity and resting-state functional connectivity by fMRI. We localized a set of six egomotion-responsive visual areas (V6+, V3A, intraparietal motion/ventral intraparietal [IPSmot/VIP], cingulate sulcus visual area [CSv], posterior cingulate sulcus area [pCi], posterior insular cortex [PIC]) by using optic flow. We tested their response to a motor task implying long-range active leg movements. Results revealed that, among these visually defined areas, CSv, pCi, and PIC responded to leg movements (visuomotor areas), while V6+, V3A, and IPSmot/VIP did not (visual areas). Functional connectivity analysis showed that visuomotor areas are connected to the cingulate motor areas, the supplementary motor area, and notably to the medial portion of the somatosensory cortex, which represents legs and feet. We suggest that CSv, pCi, and PIC perform the visual analysis of egomotion-like signals to provide sensory information to the motor system with the aim of guiding locomotion.

The dynamic contribution of the high-level visual cortex to imagery and perception.

Mental imagery and visual perception rely on the same content-dependent brain areas in the high-level visual cortex (HVC). However, little is known about dynamic mechanisms in these areas during imagery and perception. Here we disentangled local and inter-regional dynamic mechanisms underlying imagery and perception in the HVC and the hippocampus (HC), a key region for memory retrieval during imagery. Nineteen healthy participants watched or imagined a familiar scene or face during fMRI acquisition. The neural code for familiar landmarks and faces was distributed across the HVC and the HC, although with a different representational structure, and generalized across imagery and perception. However, different regional adaptation effects and inter-regional functional couplings were detected for faces and landmarks during imagery and perception. The left PPA showed opposite adaptation effects, with activity suppression following repeated observation of landmarks, but enhancement following repeated imagery of landmarks. Also, functional coupling between content-dependent brain areas of the HVC and HC changed as a function of task and content. These findings provide important information about the dynamic networks underlying imagery and perception in the HVC and shed some light upon the thin line between imagery and perception which has characterized the neuropsychological debates on mental imagery.

Hemispheric asymmetries in the transition from action preparation to execution.

Flexible and adaptive behavior requires the ability to contextually stop inappropriate actions and select the right one as quickly as possible. Recently, it has been proposed that three brain regions, i.e., the inferior frontal gyrus (iFg), the anterior insula (aIns), and the anterior intraparietal sulcus (aIPs), play an important role in several processing phases of perceptual decision tasks, especially in the preparation, perception and action phases, respectively. However, little is known about hemispheric differences in the activation of these three areas during the transition from perception to action. Many studies have examined how people prepare to stop upcoming responses through both proactive and reactive inhibitory control. Although inhibitory control has been associated with activity in the right prefrontal cortex (PFC), we have previously reported that, during a discriminative response task performed with the right hand, we observed: 1) a bilateral activity in the iFg during the preparation phase, and 2) a left dominant activity in the aIns and aIPs during the transition from perception to action, i.e., the so-called stimulus-response mapping. To clarify the hemispheric dominance of these processes, we combined the high temporal resolution of event-related potentials (ERPs) with the high spatial resolution of event-related functional magnetic resonance imaging (fMRI) while participants performed a discriminative response task (DRT) and a simple response task (SRT) using their non-dominant left hand. We confirmed that proactive inhibitory control originates in the iFg: its activity started one second before the stimulus onset and was released concomitantly to the stimulus appearance. Most importantly, we confirmed the presence of a bilateral iFg activity that seems to reflect a bilateral proactive control rather than a right-hemisphere dominance or a stronger control of the hemisphere contralateral to the responding hand. Further, we observed a stronger activation of the left aIns and a right-lateralized activation of the aIPs reflecting left-hemisphere dominance for stimulus-response mapping finalized to response execution and a contralateral-hand parietal premotor activity, respectively.

I can see where you would be: Patterns of fMRI activity reveal imagined landmarks.

Visual mental imagery arises when perceptual information is accessed from memory, originating the experience of "seeing with the mind's eye". Different content-dependent brain areas in the human ventral visual stream are activated during visual mental imagery, similarly to what happens during visual perception. The neural patterns within these regions, but not in the early visual cortex, are similar during imagery and perception, suggesting that, in the absence of perceptual stimulation, content-dependent brain areas are able to re-instantiate specific neural patterns allowing for mental imagery. However, it remains unknown whether these areas contain adequate neural representations that create mental images or need to interact with other regions in the brain, such as the hippocampus (HC), to access the necessary information from memory. To test this hypothesis, we used functional magnetic resonance imaging and both multivoxel pattern classification and psychophysiological interaction analyses. Participants were scanned while viewing or imagining scenes of familiar environments. We found that the identity of familiar places can be decoded from the neural patterns in the parahippocampal place area (PPA), retrosplenial complex/parieto-occipital sulcus (RSC/POS) and HC, during both imagery and perception, and that item-specific information from perceived places was re-instantiated during mental imagery of the same places and vice versa. Furthermore, the right PPA significantly interacted with the right HC and RSC/POS according to the performed task. Specifically, the functional coupling between PPA and HC was higher during mental imagery, whereas the functional coupling between PPA and RSC/POS was higher during perception. Our investigation provides an important contribution to the understanding of how the brain uses previously acquired knowledge to build a mental representation of the world.

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.

Path integration in 3D from visual motion cues: A human fMRI study.

While neural correlates of path integration on a yaw plane have been studied extensively, much less is known about path integration in three-dimensions (3D). Here we used fMRI during virtual navigation within tunnels in pseudo-3D. We found that the same visual motion stimuli are encoded differently in the brain depending on whether they represent displacements within the yaw plane or within the pitch plane. The yaw plane is more represented in the hippocampus while the pitch plane is more represented in the angular gyrus (AG) and in the posterior inferior temporal gyrus (pITG), known to be involved in 3D space encoding. In addition, a region in pITG, located just above the previous one, showed two different patterns with multi-voxel analysis, separately coding for the pitch and yaw planes. These results suggest that information encoded within pITG about the yaw plane may be exchanged with the hippocampus, while information about the pitch plane may be exchanged with the AG.

Spatiotemporal brain mapping during preparation, perception, and action.

Deciding whether to act or not to act is a fundamental cognitive function. To avoid incorrect responses, both reactive and proactive modes of control have been postulated. Little is known, however, regarding the brain implementation of proactive mechanisms, which are deployed prior to an actual need to inhibit a response. Via a combination of electrophysiological and neuroimaging measures (recorded in 21 and 16 participants, respectively), we describe the brain localization and timing of neural activity that underlies the anticipatory proactive mechanism. From these results, we conclude that proactive control originates in the inferior Frontal gyrus, is established well before stimulus perception, and is released concomitantly with stimulus appearance. Stimulus perception triggers early activity in the anterior insula and intraparietal cortex contralateral to the responding hand; these areas likely mediate the transition from perception to action. The neural activities leading to the decision to act or not to act are described in the framework of a three-stage model that includes perception, action, and anticipatory functions taking place well before stimulus onset.

Functional connectivity between posterior hippocampus and retrosplenial complex predicts individual differences in navigational ability.

Individuals vary widely in their ability to orient and navigate within the environment. Previous neuroimaging research has shown that hippocampus (HC) and scene-responsive regions (retrosplenial complex [RSC] and parahippocampal gyrus/parahippocampal place area [PPA]) were crucial for spatial orienting and navigation. Resting-state functional connectivity and a self-reported questionnaire of navigational ability were used to examine the hypothesis that the pattern of reciprocal connections between these regions reflects individual differences in spatial navigation. It was found that the functional connectivity between the posterior HC and RSC was significantly higher in good than in poor navigators. These results confirmed the crucial role of hippocampal and extra-hippocampal regions in spatial navigation and provided new insight into how spontaneous brain activity may account for individual differences in spatial ability. © 2016 Wiley Periodicals, Inc.

A penny for your thoughts! patterns of fMRI activity reveal the content and the spatial topography of visual mental images.

Visual mental imagery is a complex process that may be influenced by the content of mental images. Neuropsychological evidence from patients with hemineglect suggests that in the imagery domain environments and objects may be represented separately and may be selectively affected by brain lesions. In the present study, we used functional magnetic resonance imaging (fMRI) to assess the possibility of neural segregation among mental images depicting parts of an object, of an environment (imagined from a first-person perspective), and of a geographical map, using both a mass univariate and a multivariate approach. Data show that different brain areas are involved in different types of mental images. Imagining an environment relies mainly on regions known to be involved in navigational skills, such as the retrosplenial complex and parahippocampal gyrus, whereas imagining a geographical map mainly requires activation of the left angular gyrus, known to be involved in the representation of categorical relations. Imagining a familiar object mainly requires activation of parietal areas involved in visual space analysis in both the imagery and the perceptual domain. We also found that the pattern of activity in most of these areas specifically codes for the spatial arrangement of the parts of the mental image. Our results clearly demonstrate a functional neural segregation for different contents of mental images and suggest that visuospatial information is coded by different patterns of activity in brain areas involved in visual mental imagery.

Extinction learning is slower, weaker and less context specific after alcohol.

Alcohol is frequently involved in psychological trauma and often used by individuals to reduce fear and anxiety. We examined the effects of alcohol on fear acquisition and extinction within a virtual environment. Healthy volunteers were administered alcohol (0.4g/kg) or placebo and underwent acquisition and extinction from different viewpoints of a virtual courtyard, in which the conditioned stimulus, paired with a mild electric shock, was centrally located. Participants returned the following day to test fear recall from both viewpoints of the courtyard. Skin conductance responses were recorded as an index of conditioned fear. Successful fear acquisition under alcohol contrasted with impaired extinction learning evidenced by persistent conditioned responses (Experiment 1). Participants' impairments in extinction under alcohol correlated with impairments in remembering object-locations in the courtyard seen from one viewpoint when tested from the other viewpoint. Alcohol-induced extinction impairments were overcome by increasing the number of extinction trials (Experiment 2). However, a test of fear recall the next day showed persistent fear in the alcohol group across both viewpoints. Thus, alcohol impaired extinction rather than acquisition of fear, suggesting that extinction is more dependent than acquisition on alcohol-sensitive representations of spatial context. Overall, extinction learning under alcohol was slower, weaker and less context-specific, resulting in persistent fear at test that generalized to the extinction viewpoint. The selective effect on extinction suggests an effect of alcohol on prefrontal involvement, while the reduced context-specificity implicates the hippocampus. These findings have important implications for the use of alcohol by individuals with clinical anxiety disorders.

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.

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.