Paradoxical Influence of Hippocampal Neurogenesis on Working Memory

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2007 Mar 16

PMID 17360577

Citations 110

Authors

Michael D Saxe

Gael Malleret

Svetlana Vronskaya

Indira Mendez

A Denise Garcia

Michael V Sofroniew

Eric R Kandel

Rene Hen

Affiliations

Soon will be listed here.

Abstract

To explore the function of adult hippocampal neurogenesis, we ablated cell proliferation by using two independent and complementary methods: (i) a focal hippocampal irradiation and (ii) an inducible and reversible genetic elimination of neural progenitor cells. Previous studies using these methods found a weakening of contextual fear conditioning but no change in spatial reference memory, suggesting a supportive role for neurogenesis in some, but not all, hippocampal-dependent memory tasks. In the present study, we examined hippocampal-dependent and -independent working memory using different radial maze tasks. Surprisingly, ablating neurogenesis caused an improvement of hippocampal-dependent working memory when repetitive information was presented in a single day. These findings suggest that adult-born cells in the dentate gyrus have different, and in some cases, opposite roles in distinct types of memory.

Citing Articles

The longitudinal behavioral effects of acute exposure to galactic cosmic radiation in female C57BL/6J mice: Implications for deep space missions, female crews, and potential antioxidant countermeasures.

Yun S, Kiffer F, Bancroft G, Guzman C, Soler I, Haas H J Neurochem. 2024; 169(1):e16225.

PMID: 39318241 PMC: 11658192. DOI: 10.1111/jnc.16225.

SYK-623, a δ Opioid Receptor Inverse Agonist, Mitigates Chronic Stress-Induced Behavioral Abnormalities and Disrupted Neurogenesis.

Iwai T, Mishima R, Hirayama S, Nakajima H, Oyama M, Watanabe S J Clin Med. 2024; 13(2).

PMID: 38276114 PMC: 10817044. DOI: 10.3390/jcm13020608.

New Radiobiological Principles for the CNS Arising from Space Radiation Research.

Britten R, Limoli C Life (Basel). 2023; 13(6).

PMID: 37374076 PMC: 10303969. DOI: 10.3390/life13061293.

Effects of High-Fat and High-Fat High-Sugar Diets in the Anxiety, Learning and Memory, and in the Hippocampus Neurogenesis and Neuroinflammation of Aged Rats.

Mota B, Ramos M, Marques S, Silva A, Pereira P, Madeira M Nutrients. 2023; 15(6).

PMID: 36986100 PMC: 10053405. DOI: 10.3390/nu15061370.

Predicting progression to Alzheimer's disease with human hippocampal progenitors exposed to serum.

Maruszak A, Silajdzic E, Lee H, Murphy T, Liu B, Shi L Brain. 2023; 146(5):2045-2058.

PMID: 36703180 PMC: 10151193. DOI: 10.1093/brain/awac472.

References

Wall P, Messier C . The hippocampal formation--orbitomedial prefrontal cortex circuit in the attentional control of active memory. Behav Brain Res. 2001; 127(1-2):99-117. DOI: 10.1016/s0166-4328(01)00355-2. View

Snyder J, Kee N, Wojtowicz J . Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol. 2001; 85(6):2423-31. DOI: 10.1152/jn.2001.85.6.2423. View

Saxe M, Battaglia F, Wang J, Malleret G, David D, Monckton J . Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci U S A. 2006; 103(46):17501-6. PMC: 1859958. DOI: 10.1073/pnas.0607207103. View

Floresco S, Seamans J, Phillips A . Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci. 1997; 17(5):1880-90. PMC: 6573377. View

Lee I, Kesner R . Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav Neurosci. 2003; 117(5):1044-53. DOI: 10.1037/0735-7044.117.5.1044. View

Lee I, Kesner R . Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci. 2003; 23(4):1517-23. PMC: 6742248. View

Snyder J, Hong N, McDonald R, Wojtowicz J . A role for adult neurogenesis in spatial long-term memory. Neuroscience. 2005; 130(4):843-52. DOI: 10.1016/j.neuroscience.2004.10.009. View

Winocur G, Martin Wojtowicz J, Sekeres M, Snyder J, Wang S . Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus. 2006; 16(3):296-304. DOI: 10.1002/hipo.20163. View

Doetsch F, Hen R . Young and excitable: the function of new neurons in the adult mammalian brain. Curr Opin Neurobiol. 2005; 15(1):121-8. DOI: 10.1016/j.conb.2005.01.018. View

10.

Johnson W, Ruppe M, Rockenstein E, Price J, Sarthy V, Verderber L . Indicator expression directed by regulatory sequences of the glial fibrillary acidic protein (GFAP) gene: in vivo comparison of distinct GFAP-lacZ transgenes. Glia. 1995; 13(3):174-84. DOI: 10.1002/glia.440130304. View

11.

Dudchenko P . An overview of the tasks used to test working memory in rodents. Neurosci Biobehav Rev. 2004; 28(7):699-709. DOI: 10.1016/j.neubiorev.2004.09.002. View

12.

JARRARD L . On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol. 1993; 60(1):9-26. DOI: 10.1016/0163-1047(93)90664-4. View

13.

Leuner B, Gould E, Shors T . Is there a link between adult neurogenesis and learning?. Hippocampus. 2006; 16(3):216-24. DOI: 10.1002/hipo.20153. View

14.

Shors T, Townsend D, Zhao M, Kozorovitskiy Y, Gould E . Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus. 2002; 12(5):578-84. PMC: 3289536. DOI: 10.1002/hipo.10103. View

15.

Becker S . A computational principle for hippocampal learning and neurogenesis. Hippocampus. 2005; 15(6):722-38. DOI: 10.1002/hipo.20095. View

16.

Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S . Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003; 301(5634):805-9. DOI: 10.1126/science.1083328. View

17.

Meshi D, Drew M, Saxe M, Ansorge M, David D, Santarelli L . Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci. 2006; 9(6):729-31. DOI: 10.1038/nn1696. View

18.

Manev R, Manev H . The meaning of mammalian adult neurogenesis and the function of newly added neurons: the "small-world" network. Med Hypotheses. 2004; 64(1):114-7. DOI: 10.1016/j.mehy.2004.05.013. View

19.

McClelland J, Goddard N . Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus. 1996; 6(6):654-65. DOI: 10.1002/(SICI)1098-1063(1996)6:6<654::AID-HIPO8>3.0.CO;2-G. View

20.

Kesner R, Lee I, Gilbert P . A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci. 2004; 15(5):333-51. DOI: 10.1515/revneuro.2004.15.5.333. View