Abstract
Activation of β-adrenoceptors in area CA1 of the hippocampus facilitates in vitro long-term potentiation (LTP) in this region. However, it is unclear if in vivo LTP in area CA1 and hippocampus-dependent learning are subjected to β-adrenergic regulation. To address this question, we investigated the effects of the β-adrenergic agonist L-isoproterenol or antagonist DL-propranolol on in vivo LTP of area CA1 and the spatial learning in Morris water maze. In the presence of L-isoproterenol (through local infusion into area CA1), the theta-pulse stimulation with the parameter of 10 Hz, 150 pulses/train, 1 train, a frequency weakly modifying synaptic strength, induced a robust LTP, and this effect was blocked when DL-propranolol was co-administered. By contrast, the theta-pulse stimulation with the parameter of 5 Hz, 150 pulses/train, 3 trains, a frequency strongly modifying synaptic strength, induced a significantly smaller LTP when DL-propranolol was administered into area CA1. Accordingly, DL-propranolol impaired the spatial learning in the water maze when infused into area CA1 20 min pretraining. Compared with control rats, the DL-propranolol-treated rats showed significantly slower learning in the water maze and subsequently exhibited poor memory retention at 24-h test. These results suggest that β-adrenoceptors in area CA1 are involved in regulating in vivo synaptic plasticity of this area and are important for spatial learning.
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References
Squire, L. R., Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans, Psychol. Rev., 1992, 99(2): 195–231.
Bliss, T. V., Collingridge, G. L. A., Synaptic model of memory: Long-term potentiation in the hippocampus, Nature, 1993, 361(6407): 31–39.
Eichenbaum, H., Otto, T., LTP and memory: Can we enhance the connection? TINS, 1993, 16(5): 163–164.
Malenka, R. C., Nicoll, R. A., Long-term potentiation-—A decade of progress? Science, 1999, 285(5435): 1870–1874.
Martin, S. J., Grimwood, P. D., Morris, R. G. M., Synaptic plasticity and memory: An evaluation of the hypothesis, Annu. Rev. Neurosci., 2000, 23: 649–711.
Morris, R. G. M., Synaptic plasticity and learning: Selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5, J. Neurosci., 1989, 9(9): 3040–3057.
Stevens, C. F. A., Million dollar question: Does LTP = memory? Neuron, 1998, 20(1): 1–2.
Brown, G. P., Blitzer, R. D., Connor, J. H. et al., Long-term potentiation induced by theta frequency stimulation is regulated by a protein phosphatase-1-operated gate, J. Neurosci., 2000, 20(21): 7880–7887.
Giovannini, M. G., Blitzer, R. D., Wong, T. et al., Mitogen-activated protein kinase regulates early phosphorylation and delayed expression of Ca2+/calmodulin-dependent protein kinase II in long-term potentiation, J. Neurosci., 2001, 21(18): 7053–7062.
Katsuki, H., Izumi, Y., Zorumski, C. F., Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region, J. Neurophysiol., 1997, 77(6): 3013–3020.
Thomas, M. J., Moody, T. D., Makhinson, M. et al., Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region, Neuron, 1996, 17(3): 475–482.
Winder, D. G., Martin, K. C., Muzzio, I. A. et al., ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors, Neuron, 1999, 24(3): 715–726.
Paxinos, G., Watson, C., The Rat Brain in Stereotaxic Coordinates, 2nd ed., San Diego: Academic Press, 1996.
Morris, R. G. M., Garrud, P., Rawlins, J. N. et al., Place navigation impaired in rats with hippocampal lesions, Nature, 1982, 297(5868): 681–683.
Morris, R. G. M., Anderson, E., Lynch, G. S. et al., Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5, Nature, 1986, 319(6056): 774–776.
Sandin, J., Nylander, I., Georgieva, J. et al., Hippocampal dynorphin B injections impair spatial learning in rats: A kappa-opioid receptor-mediated effect, Neuroscience, 1998, 85(2): 375–382.
McGaugh, J. L., Cahill, L., Roozendaal, B., Involvement of the amygdala in memory storage: Interaction with other brain systems, Proc. Natl. Acad. Sci. USA, 1996, 93(24): 13508–13514.
Ferry, B., Roozendaal, B., McGaugh, J. L., Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: A critical involvement of the amygdala, Biol. Psychiatry, 1999, 46(9): 1140–1152.
Abel, T., Nguyen, P. V., Barad, M. et al., Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory, Cell, 1997, 88(5): 615–626.
Blum, S., Moore, A. N., Adams, F. et al., A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory, J. Neurosci., 1999, 19(9): 3535–3544.
Schafe, G. E., Nadel, N. V., Sullivan, G. M. et al., Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP Kinase, Learn. Mem., 1999, 6(2): 97–110.
Selcher, J. C., Atikins, C. M., Trzaskos, J. M. et al., A necessity for MAP kinase activation in mammalian spatial learning, Learn. Mem., 1999, 6(5): 478–490.
Silva, A. J., Kogan, J. H., Frankland, P. W. et al., CREB and memory, Annu. Rev. Neurosci., 1998, 21: 127–148.
Impey, S., Obrietan, K., Storm, D. R., Making new connections: Role of ERK/MAP kinase signaling in neuronal plasticity, Neuron, 1999, 23(1): 11–14.
Kandel, E. R., The molecular biology of memory storage: A dialogue between genes and synapses, Science, 2001, 294(5544): 1030–1038.
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Ji, J., Zhang, X. & Li, B. β-adrenergic modulation of in vivo long-term potentiation in area CA1 and its role in spatial learning in rats. Sci. China Ser. C.-Life Sci. 46, 605–614 (2003). https://doi.org/10.1360/02yc0243
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DOI: https://doi.org/10.1360/02yc0243