Shared rhythmic subcortical GABAergic input to the entorhinal cortex and presubiculum
- University of Oxford, United Kingdom
Abstract
Rhythmic theta frequency (~5-12 Hz) oscillations coordinate neuronal synchrony and higher frequency oscillations across the cortex. Spatial navigation and context-dependent episodic memories are represented in several interconnected regions including the hippocampal and entorhinal cortices, but the cellular mechanisms for their dynamic coupling remain to be defined. Using monosynaptically-restricted retrograde viral tracing in mice, we identified a subcortical GABAergic input from the medial septum that terminated in the entorhinal cortex, with collaterals innervating the dorsal presubiculum. Extracellularly recording and labeling GABAergic entorhinal-projecting neurons in awake behaving mice show that these subcortical neurons, named orchid cells, fire in long rhythmic bursts during immobility and locomotion. Orchid cells discharge near the peak of hippocampal and entorhinal theta oscillations, couple to entorhinal gamma oscillations, and target subpopulations of extra-hippocampal GABAergic interneurons. Thus, orchid cells are a specialized source of rhythmic subcortical GABAergic modulation of 'upstream' and 'downstream' cortico-cortical circuits involved in mnemonic functions.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files.
Article and author information
Author details
Funding
Medical Research Council (MC_UU_12024/4)
- Tim James Viney
- Minas Salib
- Abhilasha Joshi
- Gunes Unal
- Naomi Berry
- Peter Somogyi
Wellcome (108726/Z/15/Z)
- Tim James Viney
- Minas Salib
- Abhilasha Joshi
- Gunes Unal
- Naomi Berry
- Peter Somogyi
Felix Doctoral Scholarship
- Abhilasha Joshi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Laura Colgin, The University of Texas at Austin, Center for Learning and Memory, United States
Ethics
Animal experimentation: All procedures involving experimental animals were approved by the Department of Pharmacology Animal Welfare and Ethical Review Body under approved personal and project licenses (project licence number: 30/3240) in accordance with the Animals (Scientific Procedures) Act, 1986 (UK) and associated regulations. All surgery was performed under isoflurane anesthesia with a peri-operative dose of buprenorphine, and every effort was made to minimize suffering.
Version history
- Received: December 15, 2017
- Accepted: April 4, 2018
- Accepted Manuscript published: April 5, 2018 (version 1)
- Version of Record published: April 19, 2018 (version 2)
Copyright
© 2018, Viney 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.
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Shared rhythmic subcortical GABAergic input to the entorhinal cortex and presubiculum
eLife 7:e34395.
https://doi.org/10.7554/eLife.34395
Further reading
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- Neuroscience
Asymmetries in the size of structures deep below the cortex explain how alpha oscillations in the brain respond to shifts in attention.
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- Neuroscience
Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.
