The brain dynamics of visuospatial perspective-taking captured by intracranial EEG.

Visuospatial perspective-taking (VPT) is the ability to imagine a scene from a position different from the one used in self-perspective judgments (SPJ). We typically use VPT to understand how others see the environment. VPT requires overcoming the self-perspective, and impairments in this process are implicated in various brain disorders, such as schizophrenia and autism. However, the underlying brain areas of VPT are not well distinguished from SPJ-related ones and from domain-general responses to both perspectives. In addition, hierarchical processing theory suggests that domain-specific processes emerge over time from domain-general ones. It mainly focuses on the sensory system, but outside of it, support for this hypothesis is lacking. Therefore, we aimed to spatiotemporally distinguish brain responses domain-specific to VPT from the specific ones to self-perspective, and domain-general responses to both perspectives. In particular, we intended to test whether VPT- and SPJ specific responses begin later than the general ones. We recorded intracranial EEG data from 30 patients with epilepsy who performed a task requiring laterality judgments during VPT and SPJ, and analyzed the spatiotemporal features of responses in the broad gamma band (50-150 Hz). We found VPT-specific processing in a more extensive brain network than SPJ-specific processing. Their dynamics were similar, but both differed from the general responses, which began earlier and lasted longer. Our results anatomically distinguish VPT-specific from SPJ-specific processing. Furthermore, we temporally differentiate between domain-specific and domain-general processes both inside and outside the sensory system, which serves as a novel example of hierarchical processing.

Timing of Allocentric and Egocentric Spatial Processing in Human Intracranial EEG.

Spatial reference frames (RFs) play a key role in spatial cognition, especially in perception, spatial memory, and navigation. There are two main types of RFs: egocentric (self-centered) and allocentric (object-centered). Although many fMRI studies examined the neural correlates of egocentric and allocentric RFs, they could not sample the fast temporal dynamics of the underlying cognitive processes. Therefore, the interaction and timing between these two RFs remain unclear. Taking advantage of the high temporal resolution of intracranial EEG (iEEG), we aimed to determine the timing of egocentric and allocentric information processing and describe the brain areas involved. We recorded iEEG and analyzed broad gamma activity (50-150 Hz) in 37 epilepsy patients performing a spatial judgment task in a three-dimensional circular virtual arena. We found overlapping activation for egocentric and allocentric RFs in many brain regions, with several additional egocentric- and allocentric-selective areas. In contrast to the egocentric responses, the allocentric responses peaked later than the control ones in frontal regions with overlapping selectivity. Also, across several egocentric or allocentric selective areas, the egocentric selectivity appeared earlier than the allocentric one. We identified the maximum number of egocentric-selective channels in the medial occipito-temporal region and allocentric-selective channels around the intraparietal sulcus in the parietal cortex. Our findings favor the hypothesis that egocentric spatial coding is a more primary process, and allocentric representations may be derived from egocentric ones. They also broaden the dominant view of the dorsal and ventral streams supporting egocentric and allocentric space coding, respectively.

Brain mechanisms of visuospatial perspective-taking in relation to object mental rotation and the theory of mind.

Visuospatial perspective-taking (VPT) is a process of imagining what can be seen and how a scene looks from a location and orientation in space that differs from one's own. It comprises two levels that are underpinned by distinct neurocognitive processes. Level-2 VPT is often studied in relation to two other cognitive phenomena, object mental rotation (oMR) and theory of mind (ToM). With the aim to describe the broad picture of neurocognitive processes underlying level-2 VPT, here we give an overview of the recent behavioral and neuroscientific findings of level-2 VPT. We discuss its relation to level-1 VPT, which is also referred to as perspective-tracking, and the neighboring topics, oMR and ToM. Neuroscientific research shows that level-2 VPT is a diverse cognitive process, encompassing functionally distinct neural circuits. It shares brain substrates with oMR, especially those parietal brain areas that are specialized in spatial reasoning. However, compared to oMR, level-2 VPT involves additional activations in brain structures that are typically involved in ToM tasks and deal with self/other distinctions. In addition, level-2 VPT has been suggested to engage brain areas coding for internal representations of the body. Thus, the neurocognitive model underpinning level-2 VPT can be understood as a combination of visuospatial processing with social cognition and body schema representations.