Learning differentially shapes prefrontal and hippocampal activity during classical conditioning.

Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE

Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012-

Conditioning, Classical* ; Learning*; Hippocampus/*physiology ; Mice/*physiology ; Prefrontal Cortex/*physiology; Animals ; Male ; Mice, Inbred C57BL

The ability to use sensory cues to inform goal-directed actions is a critical component of behavior. To study how sounds guide anticipatory licking during classical conditioning, we employed high-density electrophysiological recordings from the hippocampal CA1 area and the prefrontal cortex (PFC) in mice. CA1 and PFC neurons undergo distinct learning-dependent changes at the single-cell level and maintain representations of cue identity at the population level. In addition, reactivation of task-related neuronal assemblies during hippocampal awake Sharp-Wave Ripples (aSWRs) changed within individual sessions in CA1 and over the course of multiple sessions in PFC. Despite both areas being highly engaged and synchronized during the task, we found no evidence for coordinated single cell or assembly activity during conditioning trials or aSWR. Taken together, our findings support the notion that persistent firing and reactivation of task-related neural activity patterns in CA1 and PFC support learning during classical conditioning.
Competing Interests: JK, BS, FB No competing interests declared
(© 2021, Klee et al.)

PLoS Biol. 2005 Dec;3(12):e402. (PMID: 16279838)
J Neurosci. 2016 Nov 23;36(47):12010-12026. (PMID: 27881785)
J Neurophysiol. 1997 Aug;78(2):1030-44. (PMID: 9307133)
Curr Biol. 2018 Jan 8;28(1):R37-R50. (PMID: 29316421)
Nat Rev Neurosci. 2018 Dec;19(12):744-757. (PMID: 30356103)
J Neurosci Methods. 2013 Nov 15;220(2):149-66. (PMID: 23639919)
Nature. 2015 Jun 18;522(7556):309-14. (PMID: 26053122)
Nature. 2010 Apr 1;464(7289):763-7. (PMID: 20360742)
J Neurosci. 2014 Jan 22;34(4):1432-45. (PMID: 24453332)
Neuron. 2018 May 2;98(3):616-629.e6. (PMID: 29656872)
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):378-83. (PMID: 23256159)
Neuron. 2019 Dec 18;104(6):1110-1125.e7. (PMID: 31677957)
Psychol Rev. 1995 Jul;102(3):419-457. (PMID: 7624455)
Curr Biol. 2020 Apr 6;30(7):1306-1311.e4. (PMID: 32197078)
Nat Neurosci. 2009 Jul;12(7):919-26. (PMID: 19483687)
Nat Commun. 2018 Jun 7;9(1):2204. (PMID: 29880806)
Neuron. 2012 Dec 20;76(6):1057-70. (PMID: 23259943)
Hippocampus. 2015 May;25(5):655-69. (PMID: 25515308)
Cell Rep. 2021 Mar 23;34(12):108885. (PMID: 33761365)
Biophys J. 1999 Feb;76(2):691-708. (PMID: 9929474)
J Neurosci. 2003 Oct 29;23(30):9897-905. (PMID: 14586019)
Nature. 2017 Mar 2;543(7643):103-107. (PMID: 28225752)
Nat Neurosci. 2017 Nov;20(11):1643-1653. (PMID: 28967910)
Neuron. 2016 Apr 6;90(1):113-27. (PMID: 26971950)
Front Behav Neurosci. 2012 Jan 05;5:90. (PMID: 22319482)
Neuron. 2010 Jun 24;66(6):921-36. (PMID: 20620877)
Neuron. 2020 Dec 9;108(5):984-998.e9. (PMID: 32949502)
Elife. 2021 Oct 19;10:. (PMID: 34665131)
Nat Neurosci. 2013 Mar;16(3):325-31. (PMID: 23396102)
Curr Opin Neurobiol. 2016 Oct;40:161-169. (PMID: 27543753)
Nature. 2017 Mar 29;543(7647):719-722. (PMID: 28358077)
Science. 2017 Jan 13;355(6321):184-188. (PMID: 28082591)
Trends Cogn Sci. 2011 Jul;15(7):310-8. (PMID: 21696996)
Nat Neurosci. 2017 Feb;20(2):251-259. (PMID: 27941790)
Nature. 1993 Oct 21;365(6448):753-6. (PMID: 8413653)
Nature. 2019 Dec;576(7786):266-273. (PMID: 31776518)
Neuron. 2012 Nov 21;76(4):695-711. (PMID: 23177956)
Neuron. 1995 Mar;14(3):477-85. (PMID: 7695894)
J Neurosci. 2017 Dec 6;37(49):11789-11805. (PMID: 29089440)
Neurobiol Learn Mem. 2013 Feb;100:117-26. (PMID: 23267870)
Neuron. 2019 Apr 3;102(1):249-259.e4. (PMID: 30770252)
Neuron. 2014 Jan 22;81(2):402-15. (PMID: 24462101)
Behav Neurosci. 2011 Jun;125(3):318-26. (PMID: 21517143)
J Neurosci. 2017 Jun 28;37(26):6289-6298. (PMID: 28559376)
Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3543-8. (PMID: 11248114)
Trends Cogn Sci. 2018 Oct;22(10):853-869. (PMID: 30266146)
Hippocampus. 1998;8(6):638-46. (PMID: 9882021)
Neuron. 2020 Apr 8;106(1):154-165.e6. (PMID: 32032512)
Science. 2008 Nov 7;322(5903):960-3. (PMID: 18988855)
Front Behav Neurosci. 2012 Dec 04;6:84. (PMID: 23316148)
Neuron. 2017 May 17;94(4):891-907.e6. (PMID: 28521139)
Neuron. 2017 Jun 21;94(6):1248-1262.e4. (PMID: 28602691)
Behav Brain Res. 2007 Dec 11;185(1):9-20. (PMID: 17707920)
Elife. 2021 Mar 08;10:. (PMID: 33683201)
Neurobiol Learn Mem. 2013 Nov;106:343-50. (PMID: 23911917)

Keywords: CA1; PFC; conditioning; electrophysiology; mouse; neuroscience; reward; sharp-wave ripples

Date Created: 20211019 Date Completed: 20211118 Latest Revision: 20231107

20240829

PMC8545395

10.7554/eLife.65456

34665131