Cortico-hippocampal interplay: Self-organizing phase-locked loops for indexing memory

A difficulty with the connectionist idea of representation in neural networks of the mammalian brain is that a single neuron cannot make a sufficient number of connections to influence the functional organization within networks of realistic size. Although cell assemblies can form to represent individual stimuli and responses, the formation of assemblies capable of recognizing an environment as a whole is unlikely. Yet such recognition is necessary for many context-dependent types of behavior. In the present paper, a hypothesis of cortico-hippocampal interaction is suggested, which can resolve this difficulty. It involves the establishing of patterns of connectivity between the cortex and hippocampus, on the basis of temporal aspects of connectivity (i.e., axonal conduction delays) as well as spatial aspects. By means of both the available repertoire of axonal conduction delays and Hebbian processes for synaptic modification, loops of connectivity are selected which carry neural activity resonating at the frequency of the hippocampal theta rhythm. Patterns of such loops encode the environment as a whole. The relation between the hippocampal theta rhythm and both general behavior and learning processes is thus clarified.