Multimodal sensory contributions to hippocampal spatiotemporal selectivity
The hippocampal cognitive map is thought to be driven primarily by distal visual cues and self-motion cues, although other sensory cues have also been demonstrated to influence place cells. Performing controlled experiments exploring the precise role played by different sensory modalities in determining spatial representation in the hippocampus is challenging due to need to control non-specific stimuli such as scent cues and acoustic reflections.
To overcome these challenges we have developed an immersive virtual reality system for rats, in which any spatial information in these non-specific sensory cues are eliminated. The system combines full field of view visual stimuli with spatially accurate auditory stimuli to enable a variety of complex spatial tasks. To eliminate much of the subjectivity in identifiying single units in extracellular recording, an improved automated spike sorting method was developed based on existing gaussian mixture approaches.
These tools were then applied to determine whether visual cues alone are sufficient for standard place cell activity in the CA1 region of the hippocampus. Single unit activity was recorded both in virtual reality, where only visual cues and non-vestibular self-motion cues provided spatial information, and in the real world using a linear track experimental paradigm.
iiPlace cells displayed robust spatial selectivity in virtual reality, but only 20% of putative pyramidal cells were active in virtual reality, compared with 45% in the real world task. Distal visual and nonvestibular self-motion cues are thus sufficient to provide spatial selectivity, but vestibular and other sensory cues present int he real world are necessary to fully activate the place cell population. While bidirectional cells preferentially encode absolute position in the real world, they exhibited a distance coding scheme in virtual reality, suggesting that other sensory cues such as scent marks are necessary for a robust bidirectional position code.
The frequency of hippocampal theta oscillations was reduced in virtual reality, and its speed dependence abolished. Despite this, phase precession of place fields was essentially identical in the two environments. These results constrain mechanisms governing both hip- pocampal theta oscillations and the temporal code. Taken together, these results reveal cooperative and competitive interactions between sensory modalities for control over hip- pocampal spatiotemporal selectivity and theta rhythm.