Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons

Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while r...

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Vydáno v:Nature neuroscience Ročník 21; číslo 2; s. 258 - 269
Hlavní autoři: Sasaki, Takuya, Piatti, Verónica C, Hwaun, Ernie, Ahmadi, Siavash, Lisman, John E, Leutgeb, Stefan, Leutgeb, Jill K
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Nature Publishing Group 01.02.2018
Témata:
Action Potentials - physiology
Activity patterns
Animal memory
Animals
CA3 Region, Hippocampal - cytology
Dentate gyrus
Dentate Gyrus - cytology
Dentate Gyrus - injuries
Dentate Gyrus - physiology
Granule cells
Hippocampus
Male
Maze Learning - physiology
Memory tasks
Memory, Short-Term - physiology
Mental task performance
Nerve Net - physiology
Neurons
Neurons - physiology
Rats
Rats, Long-Evans
Reinforcement
Reward
Rodents
Short term memory
Spatial memory
Spatial Memory - physiology
Statistics, Nonparametric
Task complexity
Time Factors
ISSN:1097-6256, 1546-1726, 1546-1726
On-line přístup:Získat plný text
Tagy: Přidat tag
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Abstract Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
AbstractList Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We therefore asked whether DG inputs to CA3 contribute to spatial working memory by promoting SWR generation. Recordings from DG and CA3 while rats performed a dentate-dependent working memory task on an eight-arm radial maze revealed that the activity of dentate neurons and the incidence rate of SWRs both increased during reward consumption. We then found reduced reward-related CA3 SWR generation without direct input from dentate granule neurons. Furthermore, CA3 cells with place fields in not-yet-visited arms preferentially fired during SWRs at reward locations, and these prospective CA3 firing patterns were more pronounced for correct trials and were dentate-dependent. These results indicate that coordination of CA3 neuronal activity patterns by DG is necessary for the generation of neuronal firing patterns that support goal-directed behavior and memory.
Author Ahmadi, Siavash
Lisman, John E
Piatti, Verónica C
Leutgeb, Stefan
Leutgeb, Jill K
Hwaun, Ernie
Sasaki, Takuya
Author_xml – sequence: 1
  givenname: Takuya
  surname: Sasaki
  fullname: Sasaki, Takuya
  organization: Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Kawaguchi, Japan
– sequence: 2
  givenname: Verónica C
  surname: Piatti
  fullname: Piatti, Verónica C
  organization: Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA
– sequence: 3
  givenname: Ernie
  surname: Hwaun
  fullname: Hwaun, Ernie
  organization: Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA
– sequence: 4
  givenname: Siavash
  surname: Ahmadi
  fullname: Ahmadi, Siavash
  organization: Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA
– sequence: 5
  givenname: John E
  surname: Lisman
  fullname: Lisman, John E
  organization: Department of Biology, Brandeis University, Waltham, MA, USA
– sequence: 6
  givenname: Stefan
  orcidid: 0000-0003-3367-6536
  surname: Leutgeb
  fullname: Leutgeb, Stefan
  organization: Kavli Institute for Brain and Mind, University of California, San Diego, La Jolla, CA, USA
– sequence: 7
  givenname: Jill K
  orcidid: 0000-0002-2014-842X
  surname: Leutgeb
  fullname: Leutgeb, Jill K
  email: jleutgeb@ucsd.edu
  organization: Neurobiology Section and Center for Neural Circuits and Behavior, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, USA. jleutgeb@ucsd.edu
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Snippet Complex spatial working memory tasks have been shown to require both hippocampal sharp-wave ripple (SWR) activity and dentate gyrus (DG) neuronal activity. We...
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StartPage 258
SubjectTerms Action Potentials - physiology
Activity patterns
Animal memory
Animals
CA3 Region, Hippocampal - cytology
Dentate gyrus
Dentate Gyrus - cytology
Dentate Gyrus - injuries
Dentate Gyrus - physiology
Granule cells
Hippocampus
Male
Maze Learning - physiology
Memory tasks
Memory, Short-Term - physiology
Mental task performance
Nerve Net - physiology
Neurons
Neurons - physiology
Rats
Rats, Long-Evans
Reinforcement
Reward
Rodents
Short term memory
Spatial memory
Spatial Memory - physiology
Statistics, Nonparametric
Task complexity
Time Factors
Title Dentate network activity is necessary for spatial working memory by supporting CA3 sharp-wave ripple generation and prospective firing of CA3 neurons
URI https://www.ncbi.nlm.nih.gov/pubmed/29335604
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