Dendrites support formation and reactivation of sequential memories through Hebbian plasticity

Storage 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. It is currently unknown whether Hebbian learning supports the formation of memories that are structured in time. 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 have previously been shown to acquire stable long-term memories and process sequential information. The networks were equipped with voltage-based, spike-timing dependent plasticity (STDP) and were homeostatically balanced with inhibitory STDP. In the learning phase, networks were exposed to phoneme sequences and word labels, which led to the formation of overlapping cell assemblies. In the retrieval phase, networks only received phoneme sequences as input, and we measured the firing activity of the corresponding word populations. The dendritic network correctly reactivated the word populations with a success rate of 80%, including words composed of the same phonemes in a different order. The networks of point neurons reactivated only words that contained phonemes that were unique to these words and confused words with shared phonemes (success rate below 20%). These results suggest that the slow timescale and non-linearity of dendritic depolarization allowed neurons to establish connections between neural groups that were sensitive to serial order. Inhibitory STDP prevented the potentiation of connections between unrelated neural populations during learning. During retrieval, it maintained the dendrites hyperpolarized and limited the reactivation of incorrect cell assemblies. Thus, the addition of dendrites enables the encoding of temporal relations into associative memories.