Open AccessReinforcement determines the timing dependence of corticostriatal synaptic plasticity in vivo
Author(s) -
Simon D. Fisher,
Paul B. Robertson,
Melony J. Black,
Peter Redgrave,
Mark Sagar,
Wickliffe C. Abraham,
John N. J. Reynolds
Publication year - 2017
Publication title -
nature communications
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 5.559
H-Index - 365
ISSN - 2041-1723
DOI - 10.1038/s41467-017-00394-x
Subject(s) - hebbian theory , neuroscience , synaptic plasticity , reinforcement , plasticity , nonsynaptic plasticity , homosynaptic plasticity , neuroplasticity , reinforcement learning , striatum , metaplasticity , postsynaptic potential , spike timing dependent plasticity , computer science , dopamine , psychology , biology , artificial neural network , synaptic augmentation , artificial intelligence , physics , excitatory postsynaptic potential , inhibitory postsynaptic potential , social psychology , biochemistry , receptor , thermodynamics
Plasticity at synapses between the cortex and striatum is considered critical for learning novel actions. However, investigations of spike-timing-dependent plasticity (STDP) at these synapses have been performed largely in brain slice preparations, without consideration of physiological reinforcement signals. This has led to conflicting findings, and hampered the ability to relate neural plasticity to behavior. Using intracellular striatal recordings in intact rats, we show here that pairing presynaptic and postsynaptic activity induces robust Hebbian bidirectional plasticity, dependent on dopamine and adenosine signaling. Such plasticity, however, requires the arrival of a reward-conditioned sensory reinforcement signal within 2 s of the STDP pairing, thus revealing a timing-dependent eligibility trace on which reinforcement operates. These observations are validated with both computational modeling and behavioral testing. Our results indicate that Hebbian corticostriatal plasticity can be induced by classical reinforcement learning mechanisms, and might be central to the acquisition of novel actions.