Testing the Efficacy of Single-Cell Stimulation in Biasing Presubicular Head Direction Activity

Abstract

To support navigation, the firing of head direction (HD) neurons must be tightly anchored to the external space. Indeed, inputs from external landmarks can rapidly reset the preferred direction of HD cells. Landmark stimuli have often been simulated as excitatory inputs from "visual cells" (encoding landmark information) to the HD attractor network; when excitatory visual inputs are sufficiently strong, preferred directions switch abruptly to the landmark location. In the present work, we tested whether mimicking such inputs via juxtacellular stimulation would be sufficient for shifting the tuning of individual presubicular HD cells recorded in passively rotated male rats. We recorded 81 HD cells in a cue-rich environment, and evoked spikes trains outside of their preferred direction (distance range, 11-178°). We found that HD tuning was remarkably resistant to activity manipulations. Even strong stimulations, which induced seconds-long spike trains, failed to induce a detectable shift in directional tuning. HD tuning curves before and after stimulation remained highly correlated, indicating that postsynaptic activation alone is insufficient for modifying HD output. Our data are thus consistent with the predicted stability of an HD attractor network when anchored to external landmarks. A small spiking bias at the stimulus direction could only be observed in a visually deprived environment in which both average firing rates and directional tuning were markedly reduced. Based on this evidence, we speculate that, when attractor dynamics become unstable (e.g., under disorientation), the output of HD neurons could be more efficiently controlled by strong biasing stimuli. The activity of head direction (HD) cells is thought to provide the mammalian brain with an internal sense of direction. To support navigation, the firing of HD neurons must be anchored to external landmarks, a process thought to be supported by associative plasticity within the HD system. Here, we investigated these plasticity mechanisms by juxtacellular stimulation of single HD neurons in awake rats. We found that HD coding is strongly resistant to external manipulations of spiking activity. Only in a visually deprived environment was juxtacellular stimulation able to induce a small activity bias in single presubicular neurons. We propose that juxtacellular stimulation can bias HD tuning only when competing anchoring inputs are reduced or not available.

Flight-induced compass representation in the monarch butterfly heading network

“…This allowed us to rotate the butterflies by 360 in the presence of a static sun stimulus (quiescent rotation; Figure 6A; Video S6) followed by a rotation in darkness (darkness rotation). Similar to results in cockroaches 31 and rodents, 32,33 the preferred firing direction of the butterfly neurons was invariant to the presence of visual stimuli (Figures 6B-6E; V-test: p < 0.001; n = 16 neurons; V = 0.74). The persistence of the neural tuning in darkness shows that the neurons represented heading directions in quiescence.…”

Flight-induced compass representation in the monarch butterfly heading network

“…6A and Supplementary Movie 6) followed by a rotation in darkness (darkness rotation). Similar to results in cockroaches 30 and rodents 31,32 , in these conditions, the preferred firing directions of the butterfly neurons were invariant to the presence of visual stimuli (Fig. 6B-E; n = 16 neurons; V-test: p < 0.0001).…”

Behavior-dependent directional tuning in the human visual-navigation network

“…On a population level, directional activity referenced to multiple landmarks would likely be interpreted as having broader tuning curves than the stable unidirectional counterparts. While classical HD-cells integrate vestibular inputs (Cullen and Taube, 2017;Taube, 2007), which were not available in our VR-task, visual information alone is sufficient to drive HD-cell-like coding in VR (Acharya et al, 2016) and to determine its alignment to the environment (Coletta et al, 2018). Behavioral evidence further suggests that the visual environment, specifically its geometry, influences our sense of direction (Cheng, 1986;Julian et al, 2015).…”