Sequential neuromodulation of Hebbian plasticity offers mechanism for effective reward-based navigation
Abstract
Spike timing-dependent plasticity (STDP) is under neuromodulatory control, which is correlated with distinct behavioral states. Previously we reported that dopamine, a reward signal, broadens the time window for synaptic potentiation and modulates the outcome of hippocampal STDP even when applied after the plasticity induction protocol (Brzosko et al., 2015). Here we demonstrate that sequential neuromodulation of STDP by acetylcholine and dopamine offers an efficacious model of reward-based navigation. Specifically, our experimental data in mouse hippocampal slices show that acetylcholine biases STDP towards synaptic depression, whilst subsequent application of dopamine converts this depression into potentiation. Incorporating this bidirectional neuromodulation-enabled correlational synaptic learning rule into a computational model yields effective navigation towards changing reward locations, as in natural foraging behavior. Thus, temporally sequenced neuromodulation of STDP enables associations to be made between actions and outcomes and also provides a possible mechanism for aligning the time scales of cellular and behavioral learning.
Article and author information
Author details
Funding
Biotechnology and Biological Sciences Research Council (BB/N019008/1)
- Ole Paulsen
Biotechnology and Biological Sciences Research Council (BB/N013956/1)
- Claudia Clopath
Engineering and Physical Sciences Research Council (Studentship)
- Sara Zannone
- Claudia Clopath
Medical Research Council (Studentship)
- Zuzanna Brzosko
- Wolfram Schultz
- Ole Paulsen
Wellcome (95495)
- Wolfram Schultz
Wellcome (200790/Z/16/Z)
- Claudia Clopath
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Marlene Bartos, University of Freiburg, Germany
Ethics
Animal experimentation: The research was performed under the Animals (Scientific Procedures) Act 1986 Amendment Regulations 2012 following ethical review by the University of Cambridge Animal Welfare and Ethical Review Body (AWERB). The animal procedures were authorised under Project licence PPL 70/8892.
Version history
- Received: April 18, 2017
- Accepted: July 7, 2017
- Accepted Manuscript published: July 10, 2017 (version 1)
- Version of Record published: August 7, 2017 (version 2)
Copyright
© 2017, Brzosko et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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