Proc. Natl. Acad. Sci. USA 98:4166-4171, 2001.

Formation of temporal-feature maps by axonal propagation of synaptic learning

R. Kempter, C. Leibold, H. Wagner, and J. L. van Hemmen

Computational maps are of central importance to a neuronal representation of the outside world. In a map, neighboring neurons respond to similar sensory features. A well-studied example is the computational map of interaural time differences (ITDs), which is essential to sound localization in a variety of species and allows resolution of ITDs of the order of 10 microseconds. Nevertheless it is unclear how such an orderly representation of temporal features arises. We address this problem by modeling the ontogenetic development of an ITD map in the laminar nucleus of the barn owl. We show how the owl's ITD map can emerge from a combined action of homosynaptic spike-based Hebbian learning and its propagation along the presynaptic axon. In spike-based Hebbian learning, synaptic strengths are modified according to the timing of pre- and postsynaptic action potentials. In unspecific axonal learning, a synapse's modification gives rise to a factor that propagates along the presynaptic axon and affects the properties of synapses at neighboring neurons. Our results indicate that both Hebbian learning and its presynaptic propagation are necessary for map formation in the laminar nucleus but the latter can be orders of magnitude weaker than the former. We argue that the algorithm is important for the formation of computational maps, in particular, when time plays a key role.