Cortex-wide BOLD fMRI activity reflects locally-recorded slow oscillation-associated calcium waves
- Johannes Gutenberg-University Mainz, Germany
- University Hospital Münster, Germany
Abstract
Spontaneous slow oscillation-associated slow wave activity represents an internally generated state which is characterized by alternations of network quiescence and stereotypical episodes of neuronal activity - slow wave events. However, it remains unclear which macroscopic signal is related to these active periods of the slow wave rhythm. We used optic fiber-based calcium recordings of local neural populations in cortex and thalamus to detect neurophysiologically defined slow calcium waves in isoflurane anesthetized rats. The individual slow wave events were used for an event-related analysis of simultaneously acquired whole-brain BOLD fMRI. We identified BOLD responses directly related to onsets of slow calcium waves, revealing a cortex-wide BOLD correlate: the entire cortex was engaged in this specific type of slow wave activity. These findings demonstrate a direct relation of defined neurophysiological events to a specific BOLD activity pattern and were confirmed for ongoing slow wave activity by independent component and seed-based analyses.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (Fa474/5)
- Cornelius Faber
Deutsche Forschungsgemeinschaft (SFB 1080)
- Albrecht Stroh
Deutsche Forschungsgemeinschaft (SFB 1193)
- Albrecht Stroh
Deutsche Forschungsgemeinschaft (SPP 1665)
- Albrecht Stroh
Focus Program translational Neurosciences
- Miriam Schwalm
- Albrecht Stroh
Interdisciplinary Center for Clinical Research Münster (Fa3/1603,PIX)
- Cornelius Faber
Excellence Cluster Cells in Motion (EXEC 1003)
- Cornelius Faber
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jan-Marino Ramirez, Seattle Children's Research Institute and University of Washington, United States
Ethics
Animal experimentation: Animal husbandry and experimental manipulation were carried out according to animal welfare guidelines of the Westfalian Wilhelms-University and the Johannes Gutenberg-University Mainz and were approved by the Landesamt für Natur-, Verbraucher- und Umweltschutz Nordrhein-Westfalen, Recklinghausen, Germany (animal protocol number: 84-02.04.2015.A427), and the Landesuntersuchungsamt Rheinland-Pfalz, Koblenz, Germany (animal protocol number: G 14-1-040). All surgery was performed under deep isoflurane anesthesia.
Version history
- Received: April 7, 2017
- Accepted: September 14, 2017
- Accepted Manuscript published: September 15, 2017 (version 1)
- Accepted Manuscript updated: September 19, 2017 (version 2)
- Version of Record published: October 26, 2017 (version 3)
Copyright
© 2017, Schwalm 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
-
- 4,159
- views
-
- 733
- downloads
-
- 77
- 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)
Cortex-wide BOLD fMRI activity reflects locally-recorded slow oscillation-associated calcium waves
eLife 6:e27602.
https://doi.org/10.7554/eLife.27602
Further reading
-
- Neuroscience
Simultaneous measurements of neuronal activity and fMRI signals in the rat brain have shed new light on the origins of resting-state fMRI connectivity networks.
-
- Developmental Biology
- Neuroscience
Adolescence is characterized by changes in reward-related behaviors, social behaviors, and decision-making. These behavioral changes are necessary for the transition into adulthood, but they also increase vulnerability to the development of a range of psychiatric disorders. Major reorganization of the dopamine system during adolescence is thought to underlie, in part, the associated behavioral changes and increased vulnerability. Here, we utilized fast scan cyclic voltammetry and microdialysis to examine differences in dopamine release as well as mechanisms that underlie differential dopamine signaling in the nucleus accumbens (NAc) core of adolescent (P28-35) and adult (P70-90) male rats. We show baseline differences between adult and adolescent-stimulated dopamine release in male rats, as well as opposite effects of the α6 nicotinic acetylcholine receptor (nAChR) on modulating dopamine release. The α6-selective blocker, α-conotoxin, increased dopamine release in early adolescent rats, but decreased dopamine release in rats beginning in middle adolescence and extending through adulthood. Strikingly, blockade of GABAA and GABAB receptors revealed that this α6-mediated increase in adolescent dopamine release requires NAc GABA signaling to occur. We confirm the role of α6 nAChRs and GABA in mediating this effect in vivo using microdialysis. Results herein suggest a multisynaptic mechanism potentially unique to the period of development that includes early adolescence, involving acetylcholine acting at α6-containing nAChRs to drive inhibitory GABA tone on dopamine release.
