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The Journal of Neuroscience, July 19, 2006, 26(29):7723-7729; doi:10.1523/JNEUROSCI.1454-06.2006

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Behavioral/Systems/Cognitive
Dopamine D₁/D₅ Receptors Gate the Acquisition of Novel Information through Hippocampal Long-Term Potentiation and Long-Term Depression

Neal Lemon and Denise Manahan-Vaughan

Learning and Memory Research, Medical Faculty, and International Graduate School for Neuroscience, Ruhr University Bochum, 44780 Bochum, Germany

Correspondence should be addressed to Dr. Denise Manahan-Vaughan, Learning and Memory Research, Medical Faculty, Ruhr University Bochum, FNO 1/116, Universitaetsstrasse 150, 44780 Bochum, Germany. Email: dmv-igsn{at}rub.de

Hebbian learning models require that neurons are able to both strengthen and weaken their synaptic connections. Hippocampal synaptic plasticity, in the form of long-term potentiation (LTP) and long-term depression (LTD), has been implicated in both spatial memory formation as well as novelty acquisition. In addition, the ventral tegmental area–hippocampal loop has been proposed to control the entry of information into long-term memory, whereas the dopaminergic system is believed to play an important role in information acquisition and synaptic plasticity. D₁/D₅ dopamine receptors are positively coupled to adenylyl cyclase and have been to modulate certain forms of synaptic plasticity, particularly in vitro. We investigated how D₁/D₅ dopamine receptors modify long-lasting synaptic plasticity at CA1 synapses of adult freely moving rats and found that receptor activation lowered the threshold for the induction of both LTP and LTD. Specific types of learning are associated with specific types of hippocampal synaptic plasticity. We found that object-configuration learning, facilitation of late-phase LTD by object exploration, and late-phase LTP by exploration of empty space were all prevented by D₁/D₅ receptor antagonism. Furthermore, receptor antagonism prevented electrically induced late-LTP, whereas receptor activation facilitated induction of both LTP and LTD by patterned electrical stimulation. These findings suggest that the dopaminergic system, acting via D₁/D₅ receptors, gates long-term changes in synaptic strength and that these changes are a critical factor in the acquisition of novel information.

Key words: long-term depression (LTD); long-term potentiation (LTP); novelty; CA1; hippocampus; dopamine

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Received Feb. 16, 2006; revised May 26, 2006; accepted June 10, 2006.

Correspondence should be addressed to Dr. Denise Manahan-Vaughan, Learning and Memory Research, Medical Faculty, Ruhr University Bochum, FNO 1/116, Universitaetsstrasse 150, 44780 Bochum, Germany. Email: dmv-igsn{at}rub.de

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