Corticostriatal Plasticity Established by Initial Learning Persists after Behavioral Reversal
Open Access
- 5 February 2021
- journal article
- research article
- Published by Society for Neuroscience in eneuro
Abstract
The neural mechanisms that allow animals to adapt their previously learned associations in response to changes in the environment remain poorly understood. To probe the synaptic mechanisms that mediate such adaptive behavior, we trained mice on an auditory-motor reversal task, and tracked changes in the strength of corticostriatal synapses associated with the formation of learned associations. Using a ChR2-based electrophysiological assay in acute striatal slices, we measured the strength of these synapses after animals learned to pair auditory stimuli with specific actions. Here we report that the pattern of synaptic strength initially established by learning remains unchanged even when the task contingencies are reversed. Our findings reveal that synaptic changes associated with the initial acquisition of this task are not erased or over-written, and that behavioral reversal of learned associations may recruit a separate neural circuit. These results suggest a more complex role of the striatum in regulating flexible behaviors where activity of striatal neurons may vary given the behavioral contexts of specific stimulus-action associations. Significance We have established that learning a specific auditory-motor association establishes a distinct pattern of plasticity in the tonotopic projection from auditory cortex to auditory striatum in mice. The sign of this association can be read out postmortem, with nearly perfect fidelity, using electrophysiological measurements from a single acute brain slice. We then trained another cohort of mice to reverse this association after the initial training period, and measured the plasticity pattern in this circuit. Surprisingly, even after learning the new association successfully, the corticostriatal plasticity pattern represented the initial association, acquired over 2 weeks ago. Our results have implications for the role of corticostriatal plasticity in forming stimulus-action associations and understanding the neural basis of learning in adaptive behaviors.Funding Information
- NIH
- Charles A Dana Fellowship, The Dana Foundation
This publication has 38 references indexed in Scilit:
- Corticostriatal neurons in auditory cortex drive decisions during auditory discriminationNature, 2013
- Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action valueNature Neuroscience, 2012
- Linking Topography to Tonotopy in the Mouse Auditory Thalamocortical CircuitJournal of Neuroscience, 2011
- Specialization of Binaural Responses in Ventral Auditory CorticesJournal of Neuroscience, 2010
- Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitryNature, 2010
- A new perspective on the role of the orbitofrontal cortex in adaptive behaviourNature Reviews Neuroscience, 2009
- Striatal Plasticity and Basal Ganglia Circuit FunctionNeuron, 2008
- Postsynaptic Receptor Trafficking Underlying a Form of Associative LearningScience, 2005
- Anatomical traces of juvenile learning in the auditory system of adult barn owlsNature Neuroscience, 2004
- AMPA Receptor Trafficking and Synaptic PlasticityAnnual Review of Neuroscience, 2002