Medial Parietal Cortex Encodes Perceived Heading Direction in Humans

Abstract

The ability to encode and update representations of heading direction is crucial for successful navigation. In rats, head-direction cells located within the limbic system alter their firing rate in accordance with the animal's current heading. To date, however, the neural structures that underlie an allocentric or viewpoint-independent sense of direction in humans remain unknown. Here we used functional magnetic resonance imaging (fMRI) to measure neural adaptation to distinctive landmarks associated with one of four heading directions in a virtual environment. Our experiment consisted of two phases: a "learning phase," in which participants actively navigated the virtual maze; and a "test phase," in which participants viewed pairs of images from the maze while undergoing fMRI. We found that activity within the medial parietal cortex-specifically, Brodmann area 31-was modulated by learned heading, suggesting that this region contains neural populations involved in the encoding and retrieval of allocentric heading information in humans. These results are consistent with clinical case reports of patients with acquired lesions of medial posterior brain regions, who exhibit deficits in forming and recalling links between landmarks and directional information. Our findings also help to explain why navigation disturbances are commonly observed in patients with Alzheimer's disease, whose pathology typically includes the cortical region we have identified as being crucial for maintaining representations of heading direction.

Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation

“…Head direction cells have also been observed in the rodent RSC (Chen et al, 1994;Cho and Sharp, 2001), suggesting that this region could support tracking head orientation. Recent human neuroimaging studies have indicated the RSC integrates self-motion cues during navigation with routebased spatial information (Wolbers and Buchel, 2005), directs movement towards a goal location (Epstein, 2008), and is sensitive to heading direction (Baumann and Mattingley, 2010;Marchette et al, 2014). Functional connections found here between optic flow sensitive regions and the RSC further establish a role for the RSC in updating position and orientation based on visual cues from optic flow.…”

“…During FPP navigation compared with the ITI, increased functional connectivity was observed between regions of the brain that are sensitive to optic flow motion and the retrosplenial cortex, posterior parietal cortex, hippocampus, and medial prefrontal cortex, which are brain regions previously noted in human navigational studies (Wolbers et al, 2007;Spiers and Maguire, 2007;Brown et al, 2010;Baumann and Mattingley, 2010;Doeller et al, 2010;Brown and Stern, 2014;Sherrill et al, 2013). For a summary of all brain regions showing significant functional connectivity with V3A, V6, and hMT+ seed regions at the whole-brain level for FPP navigation, see Tables 1, 2, and 3, respectively.…”

Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice

“…In humans, neuroimaging and neuropsychological work suggests that place recognition is primarily mediated by the parahippocampal place area (PPA), a region of medial occipitotemporal cortex that responds strongly when subjects view environmental scenes or landmark objects (21-23), whereas heading retrieval is primarily mediated by a system centered around the retrosplenial complex (RSC) in the medial parietal lobe (24)(25)(26)(27)(28). Analogous to the current findings, the PPA appears to be sensitive to both geometric and nongeometric information (22,(29)(30)(31)(32)(33), whereas RSC appears to be especially sensitive to geometry when people retrieve spatial information from memory (28).…”

Path integration in tactile perception of shapes

“…Since many of the traditionally thought unimodal neural circuits recently turn out to be multimodal, one hypothesis might be that the neural mechanism for whole-body navigation in the ambulatory space might perform also tactile path integration in the manipulatory space. In addition to the hippocampus and the entorhinal cortex, the medial and the posterior part of the parietal cortex, which are involved in somatosensory processing, spatial orientation, and navigation [37][38][39], might be good candidates as neuroanatomical substrate.…”