A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial remapping and grid cell field-to-field variability
Abstract
The representation of position in the mammalian brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. In addition, our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.
Data availability
This is a theoretical manuscript which does not contain data of our own. The rat trajectory used in Figure 4 to generate a distribution of velocities is taken from Fig.2c in (Hafting et al., 2005). It is available online at https://doi.org/10.11582/2014.00001.
-
Grid cell data Hafting et al 2005NIRD Research Data Archive, doi:10.11582/2014.00001.
Article and author information
Author details
Funding
Israel Science Foundation (1745/18 and 1978/13)
- Haggai Agmon
- Yoram Burak
German-Israeli Foundation for Scientific Research and Development (I-1477-421.13/2018)
- Haggai Agmon
- Yoram Burak
Gatsby Charitable Foundation (Gatsby Program in Theoretical Neuroscience at the Hebrew University)
- Haggai Agmon
- Yoram Burak
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2020, Agmon & Burak
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.
Metrics
-
- 3,652
- views
-
- 517
- downloads
-
- 40
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Two-photon (2P) fluorescence imaging through gradient index (GRIN) lens-based endoscopes is fundamental to investigate the functional properties of neural populations in deep brain circuits. However, GRIN lenses have intrinsic optical aberrations, which severely degrade their imaging performance. GRIN aberrations decrease the signal-to-noise ratio (SNR) and spatial resolution of fluorescence signals, especially in lateral portions of the field-of-view (FOV), leading to restricted FOV and smaller number of recorded neurons. This is especially relevant for GRIN lenses of several millimeters in length, which are needed to reach the deeper regions of the rodent brain. We have previously demonstrated a novel method to enlarge the FOV and improve the spatial resolution of 2P microendoscopes based on GRIN lenses of length <4.1 mm (Antonini et al., 2020). However, previously developed microendoscopes were too short to reach the most ventral regions of the mouse brain. In this study, we combined optical simulations with fabrication of aspherical polymer microlenses through three-dimensional (3D) microprinting to correct for optical aberrations in long (length >6 mm) GRIN lens-based microendoscopes (diameter, 500 µm). Long corrected microendoscopes had improved spatial resolution, enabling imaging in significantly enlarged FOVs. Moreover, using synthetic calcium data we showed that aberration correction enabled detection of cells with higher SNR of fluorescent signals and decreased cross-contamination between neurons. Finally, we applied long corrected microendoscopes to perform large-scale and high-precision recordings of calcium signals in populations of neurons in the olfactory cortex, a brain region laying approximately 5 mm from the brain surface, of awake head-fixed mice. Long corrected microendoscopes are powerful new tools enabling population imaging with unprecedented large FOV and high spatial resolution in the most ventral regions of the mouse brain.
-
- Neuroscience
Although recent studies suggest that activity in the motor cortex, in addition to generating motor outputs, receives substantial information regarding sensory inputs, it is still unclear how sensory context adjusts the motor commands. Here, we recorded population neural activity in the motor cortex via microelectrode arrays while monkeys performed flexible manual interceptions of moving targets. During this task, which requires predictive sensorimotor control, the activity of most neurons in the motor cortex encoding upcoming movements was influenced by ongoing target motion. Single-trial neural states at the movement onset formed staggered orbital geometries, suggesting that target motion modulates peri-movement activity in an orthogonal manner. This neural geometry was further evaluated with a representational model and recurrent neural networks (RNNs) with task-specific input-output mapping. We propose that the sensorimotor dynamics can be derived from neuronal mixed sensorimotor selectivity and dynamic interaction between modulations.