Dendrites support formation and reactivation of sequential memories through Hebbian plasticity

Abstract

AbstractStorage and retrieval of sequences require memory that is sensitive to the temporal order of features. For example, in human language, words that are stored in long-term memory are retrieved based on the order of phonemes (“/b/^/t/” versus “/t/^/b/“). It is unknown whether Hebbian learning supports the formation of memories structured in time. Here, we investigated whether word-like memories can emerge in a network of neurons with dendritic structures. Dendrites provide neuronal processing memory on the order of 100 ms and have been implicated in structured memory formation. We compared a network of neurons with dendrites and two networks of point neurons that has previously been shown to acquire stable long-term memories and process sequential information. The networks implemented voltage-based spike-timing dependent plasticity (STDP) and were homeostatically balanced with inhibitory STDP. In the learning phase, networks were exposed to phonemes and words represented as overlapping cell populations. In the retrieval phase, networks only received phoneme sequences as input, and we measured the reactivation of the corresponding word populations. The dendritic network correctly reactivated the word populations with a success rate of 90%, including words composed of the same phonemes in different order. The networks of point neurons reactivated only words that contained phonemes unique to that word and confused words with shared phonemes (success rate below 20%). These results indicate that the slow timescale and non-linearity of dendritic depolarization allowed dendrites toX establish connections between neural groups that were sensitive to serial order. In addition, inhibitory STDP prevented the potentiation of connections between unrelated neuronal groups during learning. During retrieval it reduced activation of words with the same phonemes in a different order. Thus, the model shows that the inclusion of dendrites enables the encoding of temporal relations into associative memories.