Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex
Abstract
Neurons of the medial entorhinal cortex (MEC) provide spatial representations critical for navigation. In this network, the periodic firing fields of grid cells act as a metric element for position. The location of the grid firing fields depends on interactions between self-motion information, geometrical properties of the environment and nonmetric contextual cues. Here, we test whether visual information, including nonmetric contextual cues, also regulates the firing rate of MEC neurons. Removal of visual landmarks caused a profound impairment in grid cell periodicity. Moreover, the speed code of MEC neurons changed in darkness and the activity of border cells became less confined to environmental boundaries. Half of the MEC neurons changed their firing rate in darkness. Manipulations of nonmetric visual cues that left the boundaries of a 1D environment in place caused rate changes in grid cells. These findings reveal context specificity in the rate code of MEC neurons.
Data availability
-
Data from: Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortexAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (AL 1730/1-1)
- Kevin Allen
Deutsche Forschungsgemeinschaft (SFB 1134)
- Kevin Allen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Howard Eichenbaum, Boston University, United States
Ethics
Animal experimentation: All experiments were carried out in accordance with the European Committees Directive (86/609/EEC) and were approved by the Governmental Supervisory Panel on Animal Experiments of Baden-Württemberg at Karlsruhe (35-9185.81/G-113/10). Every effort was made to minimize suffering.
Version history
- Received: April 14, 2016
- Accepted: July 21, 2016
- Accepted Manuscript published: July 23, 2016 (version 1)
- Version of Record published: August 16, 2016 (version 2)
Copyright
© 2016, Pérez-Escobar 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.
Metrics
-
- 4,608
- Page views
-
- 1,007
- Downloads
-
- 76
- Citations
Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.
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
Memory formation depends on neural activity across a network of regions, including the hippocampus and broader medial temporal lobe (MTL). Interactions between these regions have been studied indirectly using functional MRI, but the bases for interregional communication at a cellular level remain poorly understood. Here, we evaluate the hypothesis that oscillatory currents in the hippocampus synchronize the firing of neurons both within and outside the hippocampus. We recorded extracellular spikes from 1854 single- and multi-units simultaneously with hippocampal local field potentials (LFPs) in 28 neurosurgical patients who completed virtual navigation experiments. A majority of hippocampal neurons phase-locked to oscillations in the slow (2–4 Hz) or fast (6–10 Hz) theta bands, with a significant subset exhibiting nested slow theta × beta frequency (13–20 Hz) phase-locking. Outside of the hippocampus, phase-locking to hippocampal oscillations occurred only at theta frequencies and primarily among neurons in the entorhinal cortex and amygdala. Moreover, extrahippocampal neurons phase-locked to hippocampal theta even when theta did not appear locally. These results indicate that spike-time synchronization with hippocampal theta is a defining feature of neuronal activity in the hippocampus and structurally connected MTL regions. Theta phase-locking could mediate flexible communication with the hippocampus to influence the content and quality of memories.
-
- Developmental Biology
- Neuroscience
Down syndrome (DS) is characterized by skeletal and brain structural malformations, cognitive impairment, altered hippocampal metabolite concentration and gene expression imbalance. These alterations were usually investigated separately, and the potential rescuing effects of green tea extracts enriched in epigallocatechin-3-gallate (GTE-EGCG) provided disparate results due to different experimental conditions. We overcame these limitations by conducting the first longitudinal controlled experiment evaluating genotype and GTE-EGCG prenatal chronic treatment effects before and after treatment discontinuation. Our findings revealed that the Ts65Dn mouse model reflected the pleiotropic nature of DS, exhibiting brachycephalic skull, ventriculomegaly, neurodevelopmental delay, hyperactivity, and impaired memory robustness with altered hippocampal metabolite concentration and gene expression. GTE-EGCG treatment modulated most systems simultaneously but did not rescue DS phenotypes. On the contrary, the treatment exacerbated trisomic phenotypes including body weight, tibia microarchitecture, neurodevelopment, adult cognition, and metabolite concentration, not supporting the therapeutic use of GTE-EGCG as a prenatal chronic treatment. Our results highlight the importance of longitudinal experiments assessing the co-modulation of multiple systems throughout development when characterizing preclinical models in complex disorders and evaluating the pleiotropic effects and general safety of pharmacological treatments.