Locus Coeruleus Activation Facilitates Memory Encoding and Induces Hippocampal LTD That Depends on Beta-adrenergic Receptor Activation

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2009 May 14

PMID 19435710

Citations 60

Authors

Neal Lemon

Selcen Aydin-Abidin

Klaus Funke

Denise Manahan-Vaughan

Affiliations

Soon will be listed here.

Abstract

Spatial memory formation is enabled through synaptic information processing, in the form of persistent strengthening and weakening of synapses, within the hippocampus. It is, however, unclear how relevant spatial information is selected for encoding, in preference to less pertinent information. As the noradrenergic locus coeruleus (LC) becomes active in response to novel experiences, we hypothesized that the LC may provide the saliency signal required to promote hippocampal encoding of relevant information through changes in synaptic strength. Test pulse stimulation evoked stable basal synaptic transmission at Schaffer collateral (SC)-CA1 stratum radiatum synapses in freely behaving adult rats. Coupling of these test pulses with electrical stimulation of the LC induced long-term depression (LTD) at SC-CA1 synapses and induced a transient suppression of theta-frequency oscillations. Effects were N-methyl-D-aspartate and beta-adrenergic receptor dependent. Activation of the LC also increased CA1 noradrenalin levels and facilitated the encoding of spatial memory for a single episode via a beta-adrenoceptor-dependent mechanism. Our results demonstrate that the LC plays a key role in the induction of hippocampal LTD and in promoting the encoding of spatial information. This LC-hippocampal interaction may reflect a means by which salient information is distinguished for subsequent synaptic processing.

Citing Articles

The Modulation by the Locus Coeruleus of Recent and Remote Memory Retrieval is Activity-Dependent.

Babushkina N, Manahan-Vaughan D Hippocampus. 2025; 35(2):e70004.

PMID: 39980081 PMC: 11842585. DOI: 10.1002/hipo.70004.

Unraveling the functional complexity of the locus coeruleus-norepinephrine system: insights from molecular anatomy to neurodynamic modeling.

Su C, Yang F, Lai R, Li Y, Naeem H, Yao N Cogn Neurodyn. 2025; 19(1):29.

PMID: 39866663 PMC: 11757662. DOI: 10.1007/s11571-024-10208-8.

Oppositional and competitive instigation of hippocampal synaptic plasticity by the VTA and locus coeruleus.

Hagena H, Manahan-Vaughan D Proc Natl Acad Sci U S A. 2025; 122(1):e2402356122.

PMID: 39793037 PMC: 11725844. DOI: 10.1073/pnas.2402356122.

Hippocampal contextualization of social rewards in mice.

Duarte J, Nguyen R, Kyprou M, Li K, Milentijevic A, Cerquetella C Nat Commun. 2024; 15(1):9493.

PMID: 39489746 PMC: 11532361. DOI: 10.1038/s41467-024-53866-2.

Cannabinoids and monoaminergic system: implications for learning and memory.

Zhao S, Gu Z, Yue Y, Zhang X, Dong Y Front Neurosci. 2024; 18:1425532.

PMID: 39206116 PMC: 11349573. DOI: 10.3389/fnins.2024.1425532.

References

Whitlock J, Heynen A, Shuler M, Bear M . Learning induces long-term potentiation in the hippocampus. Science. 2006; 313(5790):1093-7. DOI: 10.1126/science.1128134. View

Bear M, Abraham W . Long-term depression in hippocampus. Annu Rev Neurosci. 1996; 19:437-62. DOI: 10.1146/annurev.ne.19.030196.002253. View

Duffy S, Craddock K, Abel T, Nguyen P . Environmental enrichment modifies the PKA-dependence of hippocampal LTP and improves hippocampus-dependent memory. Learn Mem. 2001; 8(1):26-34. PMC: 311356. DOI: 10.1101/lm.36301. View

Pavlides C, Greenstein Y, Grudman M, WINSON J . Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 1988; 439(1-2):383-7. DOI: 10.1016/0006-8993(88)91499-0. View

Martin S, Grimwood P, Morris R . Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci. 2000; 23:649-711. DOI: 10.1146/annurev.neuro.23.1.649. View

Kart-Teke E, de Souza Silva M, Huston J, Dere E . Wistar rats show episodic-like memory for unique experiences. Neurobiol Learn Mem. 2005; 85(2):173-82. DOI: 10.1016/j.nlm.2005.10.002. View

Huerta P, Lisman J . Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature. 1993; 364(6439):723-5. DOI: 10.1038/364723a0. View

Sara S, Roullet P, PRZYBYSLAWSKI J . Consolidation of memory for odor-reward association: beta-adrenergic receptor involvement in the late phase. Learn Mem. 1999; 6(2):88-96. PMC: 311281. View

Oomura Y, Hori N, Shiraishi T, Fukunaga K, Takeda H, Tsuji M . Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides. 2006; 27(11):2738-49. DOI: 10.1016/j.peptides.2006.07.001. View

10.

Gelinas J, L Banko J, Hou L, Sonenberg N, Weeber E, Klann E . ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J Biol Chem. 2007; 282(37):27527-27535. DOI: 10.1074/jbc.M701077200. View

11.

Kemp A, Manahan-Vaughan D . Hippocampal long-term depression: master or minion in declarative memory processes?. Trends Neurosci. 2007; 30(3):111-8. DOI: 10.1016/j.tins.2007.01.002. View

12.

Morris R . Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci. 2006; 23(11):2829-46. DOI: 10.1111/j.1460-9568.2006.04888.x. View

13.

Johnson M . The beta-adrenoceptor. Am J Respir Crit Care Med. 1998; 158(5 Pt 3):S146-53. DOI: 10.1164/ajrccm.158.supplement_2.13tac110. View

14.

Manahan-Vaughan D . Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci. 1997; 17(9):3303-11. PMC: 6573649. View

15.

Lemon N, Manahan-Vaughan D . Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci. 2006; 26(29):7723-9. PMC: 6674280. DOI: 10.1523/JNEUROSCI.1454-06.2006. View

16.

Babb S, Crystal J . Episodic-like memory in the rat. Curr Biol. 2006; 16(13):1317-21. DOI: 10.1016/j.cub.2006.05.025. View

17.

Harley C . Noradrenergic and locus coeruleus modulation of the perforant path-evoked potential in rat dentate gyrus supports a role for the locus coeruleus in attentional and memorial processes. Prog Brain Res. 1991; 88:307-21. DOI: 10.1016/s0079-6123(08)63818-2. View

18.

Manns J, Zilli E, Ong K, Hasselmo M, Eichenbaum H . Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem. 2006; 87(1):9-20. DOI: 10.1016/j.nlm.2006.05.007. View

19.

Kemp A, Manahan-Vaughan D . Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A. 2004; 101(21):8192-7. PMC: 419579. DOI: 10.1073/pnas.0402650101. View

20.

Gelinas J, Nguyen P . Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci. 2005; 25(13):3294-303. PMC: 6724894. DOI: 10.1523/JNEUROSCI.4175-04.2005. View