Abstract
The corticostriatal circuit has been identified as a vital pathway for associative learning. However, how learning is implemented when the sensory striatum is permanently impaired remains unclear. Using chemogenetic techniques to suppress layer five auditory cortex (AC) input to the auditory striatum, learning of a sound discrimination task was significantly impacted in freely moving Mongolian gerbils, in particular when this suppression occurs early on during learning. Whole-cell recordings sampled throughout learning revealed a transient reduction in postsynaptic (GABAA) inhibition in both striatal D1 and D2 cells in normal-hearing gerbils during task acquisition. In contrast, when the baseline striatal inhibitory strengths and firing rates were permanently reduced by a transient period of developmental sensory deprivation, learning was accompanied by augmented inhibition and increased firing rates. Direct manipulation of striatal inhibition in vivo and in vitro revealed a key role of the transient inhibitory changes in task acquisition. Together, these results reveal a flexible corticostriatal inhibitory synaptic plasticity mechanism that accompanies associative auditory learning.
Highlights
The ability of an organism to associate different stimuli from the environment with specific sets of actions is fundamental to survival
By direct manipulation of inhibitory levels during task acquisition, we found that learning could be suppressed in control animals when inhibition was maintained at a high level through local infusions of a GABAA-α2/3 subunit receptor agonist
We chemogenetically suppressed the excitatory input from layer 5 auditory cortex (AC) to the auditory striatum with an inhibitory Designer Receptors Exclusively Activated by Designer Drug
Summary
The ability of an organism to associate different stimuli from the environment with specific sets of actions is fundamental to survival. Like the rest of the basal ganglia, the auditory striatum includes two distinct populations of medium spiny neurons (MSNs), defined in part by the expression of dopamine receptor type: D1-receptor expressing (direct pathway) and D2-receptor expressing cells (indirect pathway) These MSNs receive, in majority excitatory input from AC layer 5 intratelencephalic neurons (IT) and pyramidal tract neurons (PT), respectively (Reiner et al, 2010; Cui et al, 2013; Freeze et al, 2013; Kress et al, 2013; Calabresi et al, 2014; Cazorla et al, 2014; Rock et al, 2016). Their respective roles in learning an auditory discrimination task remain unclear, especially when the auditory striatum is permanently impaired
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