The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes self-motion stimuli experienced during everyday activities remains unknown. Here we directly addressed this fundamental question by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted overall more information about translational self-motion than their regular counterparts, due to stronger nonlinearities that enabled precise spike timing including phase locking. In contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for observed functional differences between afferent classes. Together, our results indicate that irregular and regular otolith afferents may use different strategies to encode naturalistic self-motion and static head orientation relative to gravity.
All data generated or analyzed during this study are included in the manuscript and supporting files. Source data and Matlab codes have been deposited on Figshare under the URL: https://doi.org/10.6084/m9.figshare.8251613.v1
Coding strategies in the otolith system differ for translational head motion vs static orientation relative to gravityFigshare, doi:10.6084/m9.figshare.8251613.
- Kathleen E Cullen
- Maurice J Chacron
- Maurice J Chacron
- Kathleen E Cullen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Animal experimentation: All experimental protocols were approved by the McGill University Animal Care Committee (#2001-4096) and were in compliance with the guidelines of the Canadian Council on Animal Care. Two male macaque monkeys (Macaca fascicularis) were prepared for chronic extracellular recording under aseptic conditions. The surgical preparation was similar to that previously described (Dale & Cullen, 2013). Animals (aged 6 and 8 years old) were housed in pairs on a 12 hour light/dark cycle
- Joshua I Gold, University of Pennsylvania, United States
© 2019, Jamali et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angles predicting minimal versus maximal input. We investigated whether this phase dependence exists in humans using network-targeted intracranial stimulation. Intracranial local field potentials were recorded from individuals with epilepsy undergoing medically necessary stereotactic electroencephalographic recording. In each subject, biphasic bipolar direct electrical stimulation was delivered to lateral temporal sites with demonstrated connectivity to hippocampus. Lateral temporal stimulation evoked ipsilateral hippocampal potentials with distinct early and late components. Using evoked component amplitude to measure functional connectivity, we assessed whether the phase of hippocampal theta predicted relatively high versus low connectivity. We observed an increase in the continuous phase–amplitude relationship selective to the early and late components of the response evoked by lateral temporal stimulation. The maximal difference in these evoked component amplitudes occurred across 180 degrees of separation in the hippocampal theta rhythm; that is, the greatest difference in component amplitude was observed when stimulation was delivered at theta peak versus trough. The pattern of theta-phase dependence observed for hippocampus was not identified for control locations. These findings demonstrate that hippocampal receptivity to input varies with theta phase, suggesting that theta phase reflects connectivity states of human hippocampal networks. These findings confirm a putative mechanism by which neural oscillations modulate human hippocampal function.
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