Using whole-cell patch-clamp recordings in conjunction with post hoc anatomy we investigated the physiological properties of hippocampal stratum oriens and stratum pyramidale inhibitory interneurones, before and following the induction of pharmacologically evoked gamma frequency network oscillations. Prior to kainate-induced transient epochs of gamma activity, two distinct classes of oriens interneurones, oriens lacunosum-moleculare (O-LM) and trilaminar cells, showed prominent differences in their membrane and firing properties, as well as in the amplitude and kinetics of their excitatory postsynaptic events. In the active network both types of neurone received a phasic barrage of gamma frequency excitatory inputs but, due to their differential functional integration, showed clear differences in their output patterns. While O-LM cells fired intermittently at theta frequency, trilaminar interneurones discharged on every gamma cycle and showed a propensity to fire spike doublets. Two other classes of fast spiking interneurones, perisomatic targeting basket and bistratified cells, in the active network discharged predominantly single action potentials on every gamma cycle. Thus, within a locally excited network, O-LM cells are likely to provide a theta-frequency patterned output to distal dendritic segments, whereas basket and bistratified cells are involved in the generation of locally synchronous gamma band oscillations. The anatomy and output profile of trilaminar cells suggest they are involved in the projection of locally generated gamma rhythms to distal sites. Therefore a division of labour appears to exist whereby different frequencies and spatiotemporal properties of hippocampal rhythms are mediated by different interneurone subtypes.

As a structure involved in learning and memory, the hippocampus functions as a network. The functional differentiation along the longitudinal axis of the hippocampus is poorly demarcated in comparison with the transverse axis. Using patch clamp recordings in conjunction with post hoc anatomy, we have examined the pattern of connectivity and the functional differentiation along the long axis of the hippocampus. Here, we provide anatomical and physiological evidence that the prominent rhythmic network activities of the hippocampus, the behavior-specific gamma and theta oscillations, are seen predominantly along the transverse and longitudinal axes respectively. This orthogonal relationship is the result of the axonal field trajectories and the consequential interaction of the principal cells and major interneuron subtypes involved in generating each rhythm. Thus, the axonal arborization patterns of hippocampal inhibitory cells may represent a structural framework for the spatiotemporal distribution of activity observed within the hippocampus.interneurons ͉ oscillations ͉ patch clamp T he hippocampus is required for the encoding of new information and for retrieving information shortly after acquisition (1). Spatial information is coded at theta frequencies (2) by clusters of neurons segmentally distributed along the longitudinal axis of the hippocampus (3). Gamma oscillations are also generated by the hippocampus nested within these theta rhythms and are thought to be involved in transient neuronal assembly formation (4), information transmission, and storage (5).As previous observation has shown, the hippocampus is made up of multiple lamellae organized in parallel across the long axis, in which each lamella contains a functionally independent transverse circuit (6). The well defined connections between subregions along the transverse axis facilitates the investigation of crucial neurobiological processes such as network oscillatory activity in the in vitro preparation. Although the functionally segregated subregions of the long axis of the hippocampal formation may cooperate with each other during memory formation (for review, see ref. 7), morphological evidence about their interconnectivity is sparse. Although CA3 neurons connect to other CA3 neurons (8, 9), and excitation of interneurons occurs along the longitudinal axis (10), the involvement of hippocampal interneurons in the functional circuit along the longitudinal axis of hippocampus is still unclear.Interneurons serve a wide variety of functions in the brain, amongst them generating and maintaining local or large scale coherent activity (for review, see ref. 11). They also have a particularly pivotal role in driving inhibition-based rhythms, such as gamma and theta frequency network oscillations (12-16). Theta rhythms are seen as a major operational mode of the hippocampus (for review, see ref. 17), and clusters of neurons that encode information required to perform spatial and nonspatial short-term memory tasks during theta rhythms are distributed in di...