Excitability changes within transverse lamellae of dentate granule cells and their longitudinal spread following orthodromic or antidromic activation

The functional organization of the perforant path input to the dentate gyrus of the exposed hippocampus was studied in adult rabbits anesthetized with urethane and chloralose. Electrical stimulation of perforant path fibers caused excitation of granule cells along narrow, nearly transverse strips (lamellae) of tissue. Stimulation of granule cell axons (mossy fibers) in CA3 caused antidromic activation of granule cells along similar strips. Paired‐pulse stimulation revealed marked changes in granule cell excitability both within a lamella (on‐line) and for several mm off‐line along the septo‐temporal axis of the dentate gyrus. After the first pulse, granule cells were inhibited for up to about 100 ms and then facilitated for up to hundreds of ms. Feedback activity along mossy fiber collaterals exciting local inhibitory and excitatory neurons appeared to dominate in producing on‐ and off‐line inhibition and facilitation. Neurons mediating these effects could be inhibitory basket cells and other inhibitory interneurons targeting granule cells on‐ and off‐line. In addition, excitatory mossy cells with far reaching, longitudinally running axons could affect off‐line granule cells by exciting them directly or inhibit them indirectly by exciting local inhibitory interneurons. A scheme for dentate gyrus function is proposed whereby information to the dentate gyrus becomes split into interacting transverse strips of neuronal assemblies along which temporal processing occurs. A matrix of neuronal assemblies thus arises within which fragments of events and experiences is stored through the plasticity of synapses within and between the assemblies. Similar fragments may then be recognized at later times allowing memories of the whole to be created by pattern completion at subsequent computational stages in the hippocampus. © 2008 Wiley‐Liss, Inc.