Parvalbumin-positive interneurons mediate cortical-hippocampal interactions that are necessary for memory consolidation
- University of Toronto, Canada
Abstract
Following learning, increased coupling between spindle oscillations in the medial prefrontal cortex (mPFC) and ripple oscillations in the hippocampus is thought to underlie memory consolidation. However, whether learning-induced increases in ripple-spindle coupling are necessary for successful memory consolidation has not been tested directly. In order to decouple ripple-spindle oscillations, here we chemogenetically inhibited parvalbumin-positive (PV+) interneurons, since their activity is important for regulating the timing of spiking activity during oscillations. We found that contextual fear conditioning increased ripple-spindle coupling in mice. However, inhibition of PV+ cells in either CA1 or mPFC eliminated this learning-induced increase in ripple-spindle coupling without affecting ripple or spindle incidence. Consistent with the hypothesized importance of ripple-spindle coupling in memory consolidation, post-training inhibition of PV+ cells disrupted contextual fear memory consolidation. These results indicate that successful memory consolidation requires coherent hippocampal-neocortical communication mediated by PV+ cells.
Article and author information
Author details
Kaori Takehara-Nishiuchi
Funding
Canadian Institutes of Health Research (FDN143227)
- Paul W Frankland
Canadian Institutes of Health Research (MOP74650)
- Sheena A Josselyn
Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-05458)
- Kaori Takehara-Nishiuchi
Natural Sciences and Engineering Research Council of Canada (RGPIN-2014-04947)
- Blake A Richards
Natural Sciences and Engineering Research Council of Canada
- Frances Xia
Natural Sciences and Engineering Research Council of Canada
- Matthew M Tran
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All procedures in this study were approved by the Canadian Council for Animal Care (CCAC) and the Animal Care Committees at the Hospital for Sick Children and the University of Toronto.
Copyright
© 2017, Xia 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
-
- 8,745
- views
-
- 1,675
- downloads
-
- 152
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
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)
Parvalbumin-positive interneurons mediate cortical-hippocampal interactions that are necessary for memory consolidation
eLife 6:e27868.
https://doi.org/10.7554/eLife.27868
Further reading
-
- Neuroscience
A dysfunctional signaling pathway in the hippocampus has been linked to chronic pain-related memory impairment in mice.
-
- Neuroscience
Locomotion is controlled by spinal circuits that interact with supraspinal drives and sensory feedback from the limbs. These sensorimotor interactions are disrupted following spinal cord injury. The thoracic lateral hemisection represents an experimental model of an incomplete spinal cord injury, where connections between the brain and spinal cord are abolished on one side of the cord. To investigate the effects of such an injury on the operation of the spinal locomotor network, we used our computational model of cat locomotion recently published in eLife (Rybak et al., 2024) to investigate and predict changes in cycle and phase durations following a thoracic lateral hemisection during treadmill locomotion in tied-belt (equal left-right speeds) and split-belt (unequal left-right speeds) conditions. In our simulations, the ‘hemisection’ was always applied to the right side. Based on our model, we hypothesized that following hemisection the contralesional (‘intact’, left) side of the spinal network is mostly controlled by supraspinal drives, whereas the ipsilesional (‘hemisected’, right) side is mostly controlled by somatosensory feedback. We then compared the simulated results with those obtained during experiments in adult cats before and after a mid-thoracic lateral hemisection on the right side in the same locomotor conditions. Our experimental results confirmed many effects of hemisection on cat locomotion predicted by our simulations. We show that having the ipsilesional hindlimb step on the slow belt, but not the fast belt, during split-belt locomotion substantially reduces the effects of lateral hemisection. The model provides explanations for changes in temporal characteristics of hindlimb locomotion following hemisection based on altered interactions between spinal circuits, supraspinal drives, and somatosensory feedback.
