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Coherent gamma oscillations couple the amygdala and striatum during learning

Abstract

The basolateral amygdala (BLA) mediates the facilitating effects of emotions on memory. The BLA's enhancing influence extends to various types of memories, including striatal-dependent habit formation. To shed light on the underlying mechanisms, we carried out unit and local field potential (LFP) recordings in BLA, striatum, auditory cortex and intralaminar thalamus in cats trained on a stimulus-response task in which the presentation of one of two tones predicted reward delivery. The coherence of BLA, but not of cortical or thalamic, LFPs was highest with striatal gamma activity, and intra-BLA muscimol infusions selectively reduced striatal gamma power. Moreover, coupling of BLA-striatal unit activity increased when LFP gamma power was augmented. Early in training, the rewarded and unrewarded tones elicited a modest increase in coherent BLA-striatal gamma. As learning progressed, this gamma coupling selectively increased in relation to the rewarded tone. Thus, coherent gamma oscillations coordinate amygdalostriatal interactions during learning and might facilitate synaptic plasticity.

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Figure 1: Coherent gamma activity in the BLA and ventral striatum during wakefulness.
Figure 2: Intra-BLA muscimol infusions reduce striatal gamma power.
Figure 3: Gamma oscillations increase coupling between the activity of BLA and striatal neurons.
Figure 4: Progression of licking behavior during training on the stimulus-response task.
Figure 5: Learning-related changes in correlated amygdalostriatal gamma.
Figure 6: CS+-evoked increases in coherent BLA-striatal gamma parallel behavioral performance, but are not caused by motor outputs.

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Acknowledgements

This work was supported by a National Institute of Mental Health grant (RO1 MH073610) to D.Paré

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Correspondence to Denis Paré.

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Popescu, A., Popa, D. & Paré, D. Coherent gamma oscillations couple the amygdala and striatum during learning. Nat Neurosci 12, 801–807 (2009). https://doi.org/10.1038/nn.2305

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