The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms.

Some forms of synaptic plasticity depend on the temporal coincidence of presynaptic activity and postsynaptic response. This requirement is consistent with the Hebbian, or correlational, type of learning rule used in many neural network models. Recent evidence suggests that synaptic plasticity may depend in part on the production of a membrane permeant-diffusible signal so that spatial volume may also be involved in correlational learning rules. This latter form of synaptic change has been called volume learning. In both Hebbian and volume learning rules, interaction among synaptic inputs depends on the degree of coincidence of the inputs and is otherwise insensitive to their exact temporal order. Conditioning experiments and psychophysical studies have shown, however, that most animals are highly sensitive to the temporal order of the sensory inputs. Although these experiments assay the behavior of the entire animal or perceptual system, they raise the possibility that nervous systems may be sensitive to temporally ordered events at many spatial and temporal scales. We suggest here the existence of a new class of learning rule, called a predictive Hebbian learning rule, that is sensitive to the temporal ordering of synaptic inputs. We show how this predictive learning rule could act at single synaptic connections and through diffuse neuromodulatory systems.