Valentina Sulpizio

Selective role of lingual/parahippocampal gyrus and retrosplenial complex in spatial memory across viewpoint changes relative to the environmental reference frame

Remembering object locations across different views is a fundamental competence for keeping oriented in large-scale space. Here we investigated such ability by comparing encoding and retrieval of locations across viewpoint changes relative to different spatial frames of reference. We acquired functional magnetic resonance images while subjects detected target displacements across consecutive views of a familiar virtual room, reporting changes in the target absolute position in the room (stable environmental frame), changes in its position relative to a set of movable objects (unstable object-based frame), and changes relative to their point of view (control viewer-centered frame). Behavioral costs were higher for the stable environmental frame, and a cortical network including the lingual/parahippocampal gyrus (LPHG) and the retrosplenial complex (RSC) selectively encoded spatial locations relative to this frame. Several regions, including the dorsal fronto-parietal cortex and the LPHG, were modulated by the amount of experienced viewpoint change, but only the RSC was selectively modulated by the amount of viewpoint change relative to the environmental frame, thus showing a special role in coding ones own position and heading in familiar environments.

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.

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. Hum Brain Mapp 36:945–958, 2015.

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 avatars 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.

Distributed cognitive maps reflecting real distances between places and views in the human brain.

Keeping oriented in the environment is a multifaceted ability that requires knowledge of at least three pieces of information: one’s own location (“place”) and orientation (“heading”) within the environment, and which location in the environment one is looking at (“view”). We used functional magnetic resonance imaging (fMRI) in humans to examine the neural signatures of these information. Participants were scanned while viewing snapshots which varied for place, view and heading within a virtual room. We observed adaptation effects, proportional to the physical distances between consecutive places and views, in scene-responsive (retrosplenial complex and parahippocampal gyrus), fronto-parietal and lateral occipital regions. Multivoxel pattern classification of signals in scene-responsive regions and in the hippocampus allowed supra-chance decoding of place, view and heading, and revealed the existence of map-like representations, where places and views closer in physical space entailed activity patterns more similar in neural representational space. The pattern of hippocampal activity reflected both view- and place-based distances, the pattern of parahippocampal activity preferentially discriminated between views, and the pattern of retrosplenial activity combined place and view information, while the fronto-parietal cortex only showed transient effects of changes in place, view, and heading. Our findings provide evidence for the presence of map-like spatial representations which reflect metric distances in terms of both one’s own and landmark locations.

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.

Hemispheric asymmetries in the transition from action preparation to execution

Abstract 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. HighlightsProactive inhibitory control originates in the iFg.iFg activity reflects bilateral proactive control.Left aIns activity reflects stimulus‐response mapping for response execution.Contralateral aIPs contributes to motor response planning.

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.

Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity

Anatomical and functional findings in primates suggest the existence of a dedicated parieto-medial temporal pathway for spatial navigation, consisting of both direct and indirect projections from the caudal inferior parietal lobe (cIPL) to the hippocampus and the parahippocampal cortex, with indirect projections relaying through the posterior cingulate and retrosplenial cortex. This neural network is largely unexplored in humans. This study aimed at testing the existence of a parieto-medial temporal pathway for spatial navigation in humans. We explored the cortical connectivity patterns of the parahippocampal place area (PPA), the retrosplenial cortex (RSC), and the hippocampus (HC) using resting-state functional connectivity MRI. Our results demonstrate the existence of connections between the medial temporal lobe structures, i.e., PPA and HC, and the angular gyrus (AG), the human homologue of cIPL, as well as between RSC and AG. These connectivity patterns seem to reflect the direct and the indirect projections found in primates from cIPL to the medial temporal lobe. Such a result deserves feasible considerations to better understand the brain networks underpinning human spatial navigation.

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

ABSTRACT Visual mental imagery arises when perceptual information is accessed from memory, originating the experience of “seeing with the minds 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. HIGHLIGHTSPPA, RSC/POS and HC contain item‐specific information about familiar landmarks.Item‐specific information from perceived places is re‐instantiated during imagery.The right PPA showed higher connectivity with the right RSC/POS during perception.In the right hemisphere HC showed higher connectivity with PPA during imagery.