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Intracellular ATP influences synaptic plasticity in area CA1 of rat hippocampus via metabolism to adenosine and activity-dependent activation of adenosine A1 receptors
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Zur Nedden, Stephanie, Hawley, Simon, Pentland, Naomi, Hardie, D. G. (D. Grahame), Doney, Alexander S. and Frenguelli, Bruno G. (2011) Intracellular ATP influences synaptic plasticity in area CA1 of rat hippocampus via metabolism to adenosine and activity-dependent activation of adenosine A1 receptors. The Journal of Neuroscience, Vol.31 (No.16). pp. 6221-6234. doi:10.1523/JNEUROSCI.4039-10.2011 ISSN 1529-2401.
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Official URL: http://dx.doi.org/10.1523/JNEUROSCI.4039-10.2011
Abstract
The extent to which brain slices reflect the energetic status of the in vivo brain has been a subject of debate. We addressed this issue to
investigate the recovery of energetic parameters and adenine nucleotides in rat hippocampal slices and the influence this has on synaptic
transmission and plasticity.Weshow that, although adenine nucleotide levels recover appreciably within 10minof incubation, it takes 3 h
for a full recovery of the energy charge (to >= 0.93) and that incubation of brain slices at 34°C results in a significantly higher ATP/AMP
ratio and a threefold lower activity of AMP-activated protein kinase compared with slices incubated at room temperature. Supplementation
of artificial CSF with D-ribose and adenine (Rib/Ade) increased the total adenine nucleotide pool of brain slices, which, when
corrected for the influence of the dead cut edges, closely approached in vivo values. Rib/Ade did not affect basal synaptic transmission or
paired-pulse facilitation but did inhibit long-term potentiation (LTP) induced by tetanic or weak theta-burst stimulation. This decrease
in LTP was reversed by strong theta-burst stimulation or antagonizing the inhibitory adenosine A1 receptor suggesting that the elevated
tissue ATP levels had resulted in greater activity-dependent adenosine release during LTP induction. This was confirmed by direct
measurement of adenosine release with adenosine biosensors. These observations provide new insight into the recovery of adenine
nucleotides after slice preparation, the sources of loss of such compounds in brain slices, the means by which to restore them, and the
functional consequences of doing so.
Item Type: | Journal Article | ||||
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Subjects: | Q Science > QP Physiology | ||||
Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | ||||
Library of Congress Subject Headings (LCSH): | Neurophysiology, Rats -- Physiology, Adenine nucleotides | ||||
Journal or Publication Title: | The Journal of Neuroscience | ||||
Publisher: | Society for Neuroscience | ||||
ISSN: | 1529-2401 | ||||
Official Date: | 20 April 2011 | ||||
Dates: |
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Volume: | Vol.31 | ||||
Number: | No.16 | ||||
Page Range: | pp. 6221-6234 | ||||
DOI: | 10.1523/JNEUROSCI.4039-10.2011 | ||||
Status: | Peer Reviewed | ||||
Access rights to Published version: | Restricted or Subscription Access | ||||
Date of first compliant deposit: | 17 December 2015 | ||||
Date of first compliant Open Access: | 17 December 2015 | ||||
Funder: | Research into Ageing (Charitable trust), European Commission (EC) | ||||
Grant number: | LSHM-CT-2004-005272 (EC) |
Data sourced from Thomson Reuters' Web of Knowledge
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