Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats

New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes underlying certain forms of learning and memory, it has been speculated that newborn granule cells contribute to cognition. However, previous strat...

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Published in:	Learning & memory (Cold Spring Harbor, N.Y.) Vol. 16; no. 2; p. 147
Main Authors:	Jessberger, Sebastian, Clark, Robert E, Broadbent, Nicola J, Clemenson, Jr, Gregory D, Consiglio, Antonella, Lie, D Chichung, Squire, Larry R, Gage, Fred H
Format:	Journal Article
Language:	English
Published:	United States 01.02.2009
Subjects:	Animals Animals, Genetically Modified Dentate Gyrus - cytology Dentate Gyrus - growth & development Dentate Gyrus - physiology Food Preferences Form Perception - physiology Genetic Vectors Lentivirus - genetics Male Maze Learning - physiology Memory - physiology Neurons - physiology Psychomotor Performance - physiology Rats Rats, Sprague-Dawley Recognition, Psychology - physiology Social Environment Space Perception - physiology Stereotaxic Techniques Wnt Proteins - genetics Wnt Proteins - physiology
ISSN:	1549-5485, 1549-5485
Online Access:	Get more information
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Abstract	New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes underlying certain forms of learning and memory, it has been speculated that newborn granule cells contribute to cognition. However, previous strategies aiming to causally link newborn neurons with hippocampal function used ablation strategies that were not exclusive to the hippocampus or that were associated with substantial side effects, such as inflammation. We here used a lentiviral approach to specifically block neurogenesis in the dentate gyrus of adult male rats by inhibiting WNT signaling, which is critically involved in the generation of newborn neurons, using a dominant-negative WNT (dnWNT). We found a level-dependent effect of adult neurogenesis on the long-term retention of spatial memory in the water maze task, as rats with substantially reduced levels of newborn neurons showed less preference for the target zone in probe trials >2 wk after acquisition compared with control rats. Furthermore, animals with strongly reduced levels of neurogenesis were impaired in a hippocampus-dependent object recognition task. Social transmission of food preference, a behavioral test that also depends on hippocampal function, was not affected by knockdown of neurogenesis. Here we identified a role for newborn neurons in distinct aspects of hippocampal function that will set the ground to further elucidate, using experimental and computational strategies, the mechanism by which newborn neurons contribute to behavior.
AbstractList	New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes underlying certain forms of learning and memory, it has been speculated that newborn granule cells contribute to cognition. However, previous strategies aiming to causally link newborn neurons with hippocampal function used ablation strategies that were not exclusive to the hippocampus or that were associated with substantial side effects, such as inflammation. We here used a lentiviral approach to specifically block neurogenesis in the dentate gyrus of adult male rats by inhibiting WNT signaling, which is critically involved in the generation of newborn neurons, using a dominant-negative WNT (dnWNT). We found a level-dependent effect of adult neurogenesis on the long-term retention of spatial memory in the water maze task, as rats with substantially reduced levels of newborn neurons showed less preference for the target zone in probe trials >2 wk after acquisition compared with control rats. Furthermore, animals with strongly reduced levels of neurogenesis were impaired in a hippocampus-dependent object recognition task. Social transmission of food preference, a behavioral test that also depends on hippocampal function, was not affected by knockdown of neurogenesis. Here we identified a role for newborn neurons in distinct aspects of hippocampal function that will set the ground to further elucidate, using experimental and computational strategies, the mechanism by which newborn neurons contribute to behavior. New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes underlying certain forms of learning and memory, it has been speculated that newborn granule cells contribute to cognition. However, previous strategies aiming to causally link newborn neurons with hippocampal function used ablation strategies that were not exclusive to the hippocampus or that were associated with substantial side effects, such as inflammation. We here used a lentiviral approach to specifically block neurogenesis in the dentate gyrus of adult male rats by inhibiting WNT signaling, which is critically involved in the generation of newborn neurons, using a dominant-negative WNT (dnWNT). We found a level-dependent effect of adult neurogenesis on the long-term retention of spatial memory in the water maze task, as rats with substantially reduced levels of newborn neurons showed less preference for the target zone in probe trials >2 wk after acquisition compared with control rats. Furthermore, animals with strongly reduced levels of neurogenesis were impaired in a hippocampus-dependent object recognition task. Social transmission of food preference, a behavioral test that also depends on hippocampal function, was not affected by knockdown of neurogenesis. Here we identified a role for newborn neurons in distinct aspects of hippocampal function that will set the ground to further elucidate, using experimental and computational strategies, the mechanism by which newborn neurons contribute to behavior.New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes underlying certain forms of learning and memory, it has been speculated that newborn granule cells contribute to cognition. However, previous strategies aiming to causally link newborn neurons with hippocampal function used ablation strategies that were not exclusive to the hippocampus or that were associated with substantial side effects, such as inflammation. We here used a lentiviral approach to specifically block neurogenesis in the dentate gyrus of adult male rats by inhibiting WNT signaling, which is critically involved in the generation of newborn neurons, using a dominant-negative WNT (dnWNT). We found a level-dependent effect of adult neurogenesis on the long-term retention of spatial memory in the water maze task, as rats with substantially reduced levels of newborn neurons showed less preference for the target zone in probe trials >2 wk after acquisition compared with control rats. Furthermore, animals with strongly reduced levels of neurogenesis were impaired in a hippocampus-dependent object recognition task. Social transmission of food preference, a behavioral test that also depends on hippocampal function, was not affected by knockdown of neurogenesis. Here we identified a role for newborn neurons in distinct aspects of hippocampal function that will set the ground to further elucidate, using experimental and computational strategies, the mechanism by which newborn neurons contribute to behavior.
Author	Squire, Larry R Clemenson, Jr, Gregory D Gage, Fred H Consiglio, Antonella Clark, Robert E Jessberger, Sebastian Lie, D Chichung Broadbent, Nicola J
Author_xml	– sequence: 1 givenname: Sebastian surname: Jessberger fullname: Jessberger, Sebastian organization: Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, California 92037, USA – sequence: 2 givenname: Robert E surname: Clark fullname: Clark, Robert E – sequence: 3 givenname: Nicola J surname: Broadbent fullname: Broadbent, Nicola J – sequence: 4 givenname: Gregory D surname: Clemenson, Jr fullname: Clemenson, Jr, Gregory D – sequence: 5 givenname: Antonella surname: Consiglio fullname: Consiglio, Antonella – sequence: 6 givenname: D Chichung surname: Lie fullname: Lie, D Chichung – sequence: 7 givenname: Larry R surname: Squire fullname: Squire, Larry R – sequence: 8 givenname: Fred H surname: Gage fullname: Gage, Fred H
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/19181621$$D View this record in MEDLINE/PubMed
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Snippet	New granule cells are born throughout life in the dentate gyrus of the hippocampal formation. Given the fundamental role of the hippocampus in processes...
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SubjectTerms	Animals Animals, Genetically Modified Dentate Gyrus - cytology Dentate Gyrus - growth & development Dentate Gyrus - physiology Food Preferences Form Perception - physiology Genetic Vectors Lentivirus - genetics Male Maze Learning - physiology Memory - physiology Neurons - physiology Psychomotor Performance - physiology Rats Rats, Sprague-Dawley Recognition, Psychology - physiology Social Environment Space Perception - physiology Stereotaxic Techniques Wnt Proteins - genetics Wnt Proteins - physiology
Title	Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats
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