Abstract
It is generally believed that after memory consolidation, memory-encoding synaptic circuits are persistently modified and become less plastic. This, however, may hinder the remaining capacity of information storage in a given neural circuit. Here we consider the hypothesis that memory-encoding synaptic circuits still retain reversible plasticity even after memory consolidation. To test this, we employed a protocol of auditory fear conditioning which recruited the vast majority of the thalamic input synaptic circuit to the lateral amygdala (T-LA synaptic circuit; a storage site for fear memory) with fear conditioning-induced synaptic plasticity. Subsequently the fear memory-encoding synaptic circuits were challenged with fear extinction and re-conditioning to determine whether these circuits exhibit reversible plasticity. We found that fear memory-encoding T-LA synaptic circuit exhibited dynamic efficacy changes in tight correlation with fear memory strength even after fear memory consolidation. Initial conditioning or re-conditioning brought T-LA synaptic circuit near the ceiling of their modification range (occluding LTP and enhancing depotentiation in brain slices prepared from conditioned or re-conditioned rats), while extinction reversed this change (reinstating LTP and occluding depotentiation in brain slices prepared from extinguished rats). Consistently, fear conditioning-induced synaptic potentiation at T-LA synapses was functionally reversed by extinction and reinstated by subsequent re-conditioning. These results suggest reversible plasticity of fear memory-encoding circuits even after fear memory consolidation. This reversible plasticity of memory-encoding synapses may be involved in updating the contents of original memory even after memory consolidation.
Highlights
Memory is encoded and consolidated within neural circuits in a protein-synthesis-dependent manner over time [1,2]
We have provided evidence that even after memory consolidation, initial memory-encoding T-lateral amygdala (LA) synaptic circuits can be reversibly modulated by extinction and reconditioning
Initial conditioning appears to recruit the majority of TLA synaptic circuits with learning-induced synaptic potentiation as evidenced by no significant LTP and enhanced depotentiation in brain slices after the conditioning
Summary
Memory is encoded and consolidated within neural circuits in a protein-synthesis-dependent manner over time [1,2]. Memory consolidation appears to involve the conversion of labile synaptic potentiation into a persistent increase in synaptic efficacy [4]. The belief that such persistent synaptic modifications underlie consolidated memory leads to the assumption that the synapses involved in memory encoding lose plasticity after consolidation and are less modifiable thereafter. It is yet to be demonstrated that sequential learning can recruit such reversible plasticity of memory-encoding synaptic circuits after memory consolidation, most learning-induced plasticities (i.e. LTP & LTD) are studied separately in different brain regions and learning paradigms
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