Synaptic weight dynamics underlying memory consolidation: implications for learning rules, circuit organization, and circuit function.

Systems consolidation is a common feature of learning and memory systems, in which a long-term memory initially stored in one brain region becomes persistently stored in another region. We studied the dynamics of systems consolidation in simple circuit architectures with two sites of plasticity, one in an early-learning and one in a late-learning brain area. We show that the synaptic dynamics of the circuit during consolidation of an analog memory can be understood as a temporal integration process, by which transient changes in activity driven by plasticity in the early-learning area are accumulated into persistent synaptic changes at the late-learning site. This simple principle naturally leads to a speed-accuracy tradeoff in systems consolidation and provides insight into how the circuit mitigates the stability-plasticity dilemma of storing new memories while preserving core features of older ones. Furthermore, it imposes two constraints on the circuit. First, the plasticity rule at the late-learning site must stably support a continuum of possible outputs for a given input. We show that this is readily achieved by heterosynaptic but not standard Hebbian rules. Second, to turn off the consolidation process and prevent erroneous changes at the late-learning site, neural activity in the early-learning area must be reset to its baseline activity. We propose two biologically plausible implementations for this reset that suggest novel roles for core elements of the cerebellar circuit. Significance Statement: How are memories transformed over time? We propose a simple organizing principle for how long term memories are moved from an initial to a final site of storage. We show that successful transfer occurs when the late site of memory storage is endowed with synaptic plasticity rules that stably accumulate changes in activity occurring at the early site of memory storage. We instantiate this principle in a simple computational model that is representative of brain circuits underlying a variety of behaviors. The model suggests how a neural circuit can store new memories while preserving core features of older ones, and suggests novel roles for core elements of the cerebellar circuit.