Abstract
In vitro work revealed that excitatory synaptic inputs to hippocampal inhibitory interneurons could undergo Hebbian, associative, or non-associative plasticity. Both behavioral and learning-dependent reorganization of these connections has also been demonstrated by measuring spike transmission probabilities in pyramidal cell-interneuron spike cross-correlations that indicate monosynaptic connections. Here we investigated the activity-dependent modification of these connections during exploratory behavior in rats by optogenetically inhibiting pyramidal cell and interneuron subpopulations. Light application and associated firing alteration of pyramidal and interneuron populations led to lasting changes in pyramidal-interneuron connection weights as indicated by spike transmission changes. Spike transmission alterations were predicted by the light-mediated changes in the number of pre- and postsynaptic spike pairing events and by firing rate changes of interneurons but not pyramidal cells. This work demonstrates the presence of activity-dependent associative and non-associative reorganization of pyramidal-interneuron connections triggered by the optogenetic modification of the firing rate and spike synchrony of cells.
Highlights
It is increasingly recognized that plastic reorganization of brain circuits needed for learning and other cognitive functions involves principal cells and local inhibitory interneurons (Buzsaki, 2010)
We recorded during four 25 min exploration sessions in which first a familiar environment (FAM1) was explored followed by a novel environment (NOV), and the animals were returned to the familiar environment for the remaining two sessions
A similar analysis was performed for the familiar exploration session laser stimulation was applied (FAML) session itself, where again, we found that only interneuron rate alterations predicted spike transmission alterations during the light application, even when each-others’ contribution was considered
Summary
It is increasingly recognized that plastic reorganization of brain circuits needed for learning and other cognitive functions involves principal cells and local inhibitory interneurons (Buzsaki, 2010). Our knowledge about the precise reorganization of pyramidal-interneuron connections during behavior is limited because of the technical challenge of directly performing patch-clamp recordings from monosynaptically connected pyramidal cell-interneuron pairs during such conditions Spatial learning can cause lasting changes in these connections (Dupret et al, 2013) While such studies provide strong evidence of plasticity at excitatory-interneuron synapses, so far, no data has established a causal link between pre- and postsynaptic firing to changes in connection strength during behavior. We examined whether these light-induced rate changes and the associated network effects could lead to the lasting reorganization of pyramidal-interneuron connection weights, as assessed by monosynaptic spike transmission probabilities
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