The Human Retrosplenial Cortex and Thalamus Code Head Direction in a Global Reference Frame

Abstract

Spatial navigation is a multisensory process involving integration of visual and body-based cues. In rodents, head direction (HD) cells, which are most abundant in the thalamus, integrate these cues to code facing direction. Human fMRI studies examining HD coding in virtual environments (VE) have reported effects in retrosplenial complex and (pre-)subiculum, but not the thalamus. Furthermore, HD coding appeared insensitive to global landmarks. These tasks, however, provided only visual cues for orientation, and attending to global landmarks did not benefit task performance. In the present study, participants explored a VE comprising four separate locales, surrounded by four global landmarks. To provide body-based cues, participants wore a head-mounted display so that physical rotations changed facing direction in the VE. During subsequent MRI scanning, subjects saw stationary views of the environment and judged whether their orientation was the same as in the preceding trial. Parameter estimates extracted from retrosplenial cortex and the thalamus revealed significantly reduced BOLD responses when HD was repeated. Moreover, consistent with rodent findings, the signal did not continue to adapt over repetitions of the same HD. These results were supported by a whole-brain analysis showing additional repetition suppression in the precuneus. Together, our findings suggest that: (1) consistent with the rodent literature, the human thalamus may integrate visual and body-based, orientation cues; (2) global reference frame cues can be used to integrate HD across separate individual locales; and (3) immersive training procedures providing full body-based cues may help to elucidate the neural mechanisms supporting spatial navigation.

Environmental Anchoring of Head Direction in a Computational Model of Retrosplenial Cortex

“…The present model is the first to suggest a functional role for the connection from ADN to RSC (Shibata, 1998;Vann et al, 2005). However, the complex anatomy of the RSC implies functional distinctions within RSC (e.g., visual landmark representations likely reach dysgranular RSC first, whereas HD representations enter the granular cortex) (Shibata et al, 2009;Vann et al, 2009;Sugar et al 2011). Spatially modulated HD tuning in dysgranular RSC (Jacob et al 2016) Fig.…”

“…Accordingly, allocentric (world-centered) representations of location and direction must be anchored to egocentric (bodycentered) sensory information, requiring a transformation between reference frames (Salinas and Abbott, 1995;Pouget and Sejnowski, 1997;Burgess et al, 2001a;Pouget et al, 2002;Byrne et al, 2007;Wilber et al, 2014;Alexander and Nitz, 2015). The difference between sensory input representing an egocentric landmark bearing and an allocentric HD signal can be ignored in models assuming distant orientation cues but becomes obvious in the context of motion parallax with proximal cues and in complex environments comprised of multiple connected arenas.…”

“…Coherent rotation of the preferred firing directions of HD cells in response to the displacement of visual cues, and drift in darkness (Mizumori and Williams, 1993;Goodridge et al, 1998) provide strong evidence for the attractor hypothesis. Accordingly, several models have explored various aspects of the HD system (Skaggs et al, 1995;Redish et al, 1996;Zhang, 1996;Goodridge and Touretzky, 2000;Xie et al, 2002;Hahnloser, 2003;Degris et al, 2004;Boucheny et al, 2005;Song and Wang, 2005;Stringer and Rolls, 2006;Stratton et al, 2010;.…”

“…However, sensory representations are necessarily body-centered (egocentric). The required mapping between allocentric and egocentric reference frames is a complex problem and could be addressed in terms of coordinate transforms in parietal cortex (Salinas and Abbott, 1995;Pouget and Sejnowski, 1997;Pouget et al, 2002) or retrosplenial cortex (Burgess et al, 2001a;Byrne et al, 2007, Wilber et al, 2014, Alexander and Nitz, 2015, but specific implications for the HD system have not yet been explored.…”

“…In addition, conjunctive location-by-direction coding has been found in medial enthorinal cortex (Sargolini et al, 2006), presubiculum and parasubiculum Cacucci et al, 2004;Boccara et al, 2010), and RSC Jacob et al, 2016). Lesion studies suggest that the circuitry that generates HD coding is crucially dependent on LMN and DTN.…”