Head Direction Cells in Rats with Hippocampal or Overlying Neocortical Lesions: Evidence for Impaired Angular Path Integration

Abstract

Rodents use two distinct navigation strategies that are based on environmental cues (landmark navigation) or internal cues (path integration). Head direction (HD) cells are neurons that discharge when the animal points its head in a particular direction and are responsive to the same cues that support path integration and landmark navigation. Experiment 1 examined whether HD cells in rats with lesions to the hippocampus plus the overlying neocortex or to just the overlying neocortex could maintain a stable preferred firing direction when the rats locomoted from a familiar to a novel environment, a process thought to require path integration. HD cells from both lesion groups were unable to maintain a similar preferred direction between environments, with cells from hippocampal rats showing larger shifts than cells from rats sustaining only cortical damage. When the rats first explored the novel environment, the preferred directions of the cells drifted for up to 4 min before establishing a consistent firing orientation. The preferred direction was usually maintained during subsequent visits to the novel environment but not across longer time periods (days to weeks). Experiment 2 demonstrated that a novel landmark cue was able to establish control over HD cell preferred directions in rats from both lesion groups, showing that the impairment observed in experiment 1 cannot be attributed to an impairment in establishing cue control. Experiment 3 showed that the preferred direction drifted when HD cells in lesioned animals were recorded in the dark. It was also shown that the anticipatory property of anterodorsal thalamic nucleus HD cells was still present in lesioned animals; thus, this property cannot be attributed to an intact hippocampus. These findings suggest that the hippocampus and the overlying neocortex are involved in path integration mechanisms, which enable an animal to maintain an accurate representation of its directional heading when exploring a novel environment.

Path integration in mammals

“…Contradicting these results, however, are findings reported by Alyan and McNaughton (1999) of intact PI in hippocampectomized animals, a discrepancy that has not yet been explained. Further supporting a PI role for the hippocampus, hippocampal lesions impair angular PI by head direction cells (Golob and Taube, 1999) and vestibular lesions, which disrupt the place cell representation (Taube et al, 1996), also impair path integration (Cohen, 2000;Wallace et al, 2002).…”

“…Such a cue also influences both place cells in rats (Muller and Kubie, 1987;Knierim et al, 1995;Jeffery, 1998) and homing behavior in hamsters (Etienne et al, 1996), suggesting that animals may use visual landmarks to compute their heading when they can. If, however, the visual cues are removed or otherwise unavailable (e.g., in darkness), a stable firing pattern continues to be maintained by both place cells (Quirk et al, 1990;Jeffery et al, 1997) and head direction cells (Golob and Taube, 1999), and animals can still navigate effectively (Etienne et al, 1996). Some of this ability may be supported by nonvisual environmental cues such as odors (Goodridge et al, 1998;Save et al, 2000).…”

Visual Landmark Information Gains Control of the Head Direction Signal at the Lateral Mammillary Nuclei

“…This visual input presumably originates in area 17, which may influence the HD signal via a direct projection to the PoS (Vogt and Miller, 1983). The PoS projects directly to ADN, and removal of the PoS disrupts landmark control of ADN HD cells (Goodridge and Taube, 1997), suggesting that the PoS may influence ADN HD cells via the direct PoS ¡ ADN projection (van Groen and Wyss, 1990a). However, visual information also controls the HD signal upstream from ADN, in the LMN (Blair et al, 1998;Stackman and Taube, 1998), and this visual input may arrive via the unilateral PoS ¡ LMN projection (Shibata, 1989; van Groen and Wyss, 1990a;Yoder and Taube, 2011b).…”

“…This HD cell signal appears to be generated from self-movement information that arrives from the vestibular system, but proprioceptive and/or motor efference cues also play a major role in updating the signal during movement (Taube and Burton, 1995; Blair et al, 1997; Stackman and Taube, 1997; Frohardt et al, 2006;Yoder et al, 2011a). Although these idiothetic cues are important for generating and updating the signal, visual landmarks dominantly control the preferred firing direction of the HD cell when these cues are available (Goodridge and Taube, 1995;Zugaro et al, 2003). The neural circuit responsible for providing this "landmark control" to the HD signal is not fully understood but is particularly important for our understanding of navigation and spatial learning.…”

“…Across all PoS-lesioned rats, the damaged areas ranged from 0 to 8.5% of the entire dentate gyrus. This damage is unlikely to have contributed to the HD cell responses to landmark rotations, given that complete hippocampal lesions failed to disrupt landmark control of ADN HD cells (Golob andTaube, 1997, 1999).Pairs of HD cells were simultaneously recorded on one occasion in a control rat, on one occasion in a cortex-lesioned rat, and on one occasion in a PoS-lesioned rat. The preferred firing directions of simultaneously recorded HD cells remained in register (were separated by an angular distance that remained relatively constant across sessions), and the average directional shift from both cells was used for all shift analyses.…”