Differential hippocampal and retrosplenial involvement in egocentric-updating, rotation, and allocentric processing during online spatial encoding: an fMRI study

Abstract

The way new spatial information is encoded seems to be crucial in disentangling the role of decisive regions within the spatial memory network (i.e., hippocampus, parahippocampal, parietal, retrosplenial,…). Several data sources converge to suggest that the hippocampus is not always involved or indeed necessary for allocentric processing. Hippocampal involvement in spatial coding could reflect the integration of new information generated by “online” self-related changes. In this fMRI study, the participants started by encoding several object locations in a virtual reality environment and then performed a pointing task. Allocentric encoding was maximized by using a survey perspective and an object-to-object pointing task. Two egocentric encoding conditions were used, involving self-related changes processed under a first-person perspective and implicating a self-to-object pointing task. The Egocentric-updating condition involved navigation whereas the Egocentric with rotation only condition involved orientation changes only. Conjunction analysis of spatial encoding conditions revealed a wide activation of the occipito-parieto-frontal network and several medio-temporal structures. Interestingly, only the cuneal areas were significantly more recruited by the allocentric encoding in comparison to other spatial conditions. Moreover, the enhancement of hippocampal activation was found during Egocentric-updating encoding whereas the retrosplenial activation was observed during the Egocentric with rotation only condition. Hence, in some circumstances, hippocampal and retrosplenial structures—known for being involved in allocentric environmental coding—demonstrate preferential involvement in the egocentric coding of space. These results indicate that the raw differentiation between allocentric versus egocentric representation seems to no longer be sufficient in understanding the complexity of the mechanisms involved during spatial encoding.

Structural and functional neuroplasticity in human learning of spatial routes

“…Connectivity increased between the posterior dorsal region of the human dentate gyrus (a region known to be involved in spatial learning) (Moser and Moser, 1998;Brown et al, 2014), and the right intra-parietal sulcus, right anterior and posterior temporal areas (cortical regions activated strongly in navigation and spatial memory tasks). These findings are consistent with both the anatomical connectivity among these regions (Schmahmann and Pandya, 2006), and with the functional activation of these particular cortical areas in navigation and spatial memory tasks (Gomez et al, 2014).…”

EEG correlates of spatial orientation in the human retrosplenial complex

“…The stimulus turn in the present study involved on the spot rotations, unlike previous studies that also included translations during the turn. Recent results from Gomez and colleagues showed stronger RSC activation during rotation at a fixed position compare to a continuous movement (Gomez et al, 2014).…”

“…This information is integrated with allocentric reference frames to provide information on changes in position and orientation with respect to the initial position and heading direction as long as the navigator moves in the environment or whenever the current position and orientation has to be retrieved for further computations. A second mode, reflected in modulations of the higher alpha/lower beta band (12-14 Hz), subserves the computation and maintenance of allocentric heading itself (Byrne et al, 2007;Gomez et al, 2014). This is most pronounced during actual heading changes but becomes necessary whenever allocentric heading is used to align information coded in an egocentric SRF (e.g., visual flow) that is misaligned with the allocentric heading representation.…”

Flexible egocentric and allocentric representations of heading signals in parietal cortex

“…In general, the role of the parietal cortex in navigation has been linked to egocentric representations. For example, human fMRI studies of visual navigation reported that the parietal cortex codes visual motion information in an egocentric reference frame (20)(21)(22)(23)(24)(25)(26)(27) and coactivates with the hippocampus, in which spatial maps are represented in allocentric coordinates (28)(29)(30)(31). Furthermore, rodent studies have suggested that the parietal cortex, hippocampus, and retrosplenial cortex are all involved in transformations between egocentrically and allocentrically coded information (32)(33)(34)(35).…”