Cliff Vuong | bioRxiv Science

bioRxiv2015

Visual cues determine hippocampal directional selectivity

Both spatial and directional information are necessary for navigation. Rodent hippocampal neurons show spatial selectivity in all environments1, but directional tuning only on linear paths2-8.The sensory mechanisms underlying directionality are unknown, though vestibular and visual cues are thought to be crucial. However, hippocampal neurons are thought to show no angular modulation during two-dimensional random foraging despite the presence of vestibular and visual cues6,7. Additionally, specific aspects of visual cues have not been directly linked to hippocampal responses in rodents. To resolve these issues we manipulated vestibular and visual cues in a series of experiments. We first measured hippocampal activity during random foraging in real world (RW) where we found that neurons firing exhibited significant modulation by head-direction. In fact, the fraction of modulated neurons was comparable to that in the head-direction system9. These findings are contrary to commonly held beliefs about hippocampal directionality6,7. To isolate the contribution of visual cues we measured neural responses in a visually similar virtual reality (VR) where the range of vestibular inputs is minimized5,10,11. Significant directional modulation was not only found in VR, but it was comparable to that in RW. Several additional experiments revealed that changes in the angular information contained in the visual cues induced corresponding changes in hippocampal head-directional modulation. Remarkably, for head-directionally modulated neurons, the ensemble activity was biased towards the sole visual cue. These results demonstrate that robust vestibular cues are not required for hippocampal directional selectivity, while visual cues are not only sufficient but also play a causal role in driving hippocampal responses.

Neuroscience↗

bioRxiv2013

Hippocampal Motifs

Dorsal Hippocampal neurons provide an allocentric map of space1, characterized by three key properties. First, their firing is spatially selective1-3, termed a rate code. Second, as animals traverse through place fields, neurons sustain elevated firing rates for long periods, however this has received little attention. Third the theta-phase of spikes within this sustained activity varies with animals location, termed phase-precession or a temporal code4-10. The precise relationship between these properties and the mechanisms governing them are not understood, although distal visual cues (DVC) are thought to be sufficient to reliably elicit them2,3. Hence, we measured rat CA1 neurons activity during random foraging in two-dimensional VR--where only DVC provide consistent allocentric location information-- and compared it with their activity in real world (RW). Surprisingly, we found little spatial selectivity in VR. This is in sharp contrast to robust spatial selectivity commonly seen in one-dimensional RW and VR7-11, or two-dimensional RW1-3. Despite this, neurons in VR generated approximately two-second long phase precessing spike sequences, termed \"hippocampal motifs\". Motifs, and \"Motif-fields\", an aggregation of all motifs of a neuron, had qualitatively similar properties including theta-scale temporal coding in RW and VR, but the motifs were far less spatially localized in VR. These results suggest that intrinsic, network mechanisms generate temporally coded hippocampal motifs, which can be dissociated from their spatial selectivity. Further, DVC alone are insufficient to localize motifs spatially to generate a robust rate code.

Neuroscience↗