Every neuron is part of a network, exerting its function by transforming multiple spatiotemporal synaptic input patterns into a single spiking output. This function is specified by the particular shape and passive electrical properties of the neuronal membrane, and the composition and spatial distribution of ion channels across its processes. For a variety of physiological or pathological reasons, the intrinsic input/output function may change during a neuron’s lifetime. This process results in high variability in the peak specific conductance of ion channels in individual neurons. The mechanisms responsible for this variability are not well understood, although there are clear indications from experiments and modeling that degeneracy and correlation among multiple channels may be involved. Here, we studied this issue in biophysical models of hippocampal CA1 pyramidal neurons and interneurons. Using a unified data-driven simulation workflow and starting from a set of experimental recordings and morphological reconstructions obtained from rats, we built and analyzed several ensembles of morphologically and biophysically accurate single cell models with intrinsic electrophysiological properties consistent with experimental findings. The results suggest that the set of conductances expressed in any given hippocampal neuron may be considered as belonging to two groups: one subset is responsible for the major characteristics of the firing behavior in each population and the other is responsible for a robust degeneracy. Analysis of the model neurons suggests several experimentally testable predictions related to the combination and relative proportion of the different conductances that should be expressed on the membrane of different types of neurons for them to fulfill their role in the hippocampus circuitry.

Strong constraints on the neural mechanisms underlying the formation of place fields in the rodent hippocampus come from the systematic changes in spatial activity patterns that are consequent on systematic environmental manipulations. We describe an attractor network model of area CA3 in which local, recurrent, excitatory, and inhibitory interactions generate appropriate place cell representations from location-and directionspecific activity in the entorhinal cortex.In the model, familiarity with the environment, as reflected by activity in neuromodulatory systems, influences the efficacy and plasticity of the recurrent and feedforward inputs to CA3. In unfamiliar, novel, environments, mossy fiber inputs impose activity patterns on CA3, and the recurrent collaterals and the perforant path inputs are subject to graded Hebbian plasticity.This sculpts CA3 attractors and associates them with activity patterns in the entorhinal cortex. In familiar environments, place fields are controlled by the way that perforant path inputs select among the attractors.Depending on the training experience provided, the model generates place fields that are either directional or nondirectional and whose changes when the environment undergoes simple geometric transformations are in accordance with experimental data. Representations of multiple environments can be stored and recalled with little interference, and these have the appropriate degrees of similarity in visually similar environments. Key words: hippocampus; place cells; CA3; recurrent network; plasticity; familiarity; neuromodulation; directionality; attractor; modelThe hippocampus is known to be involved in spatial learning and memory in rodents. Some of the most convincing evidence for this is the presence of place cells in areas CA3 and CA1 of the hippocampus (O' Keefe and Dostrovsky, 1971;O'Keefe, 1976) and of many other types of spatially selective cells in neighboring areas (Quirk et al., 1992;Jung and McNaughton, 1993). Principal neurons in CA3 and CA1 are active only when the animal is located in a well defined local region of the environment (a place field) and collectively provide a population code for spatial position (Wilson and McNaughton, 1993). The question we address is how this comes to be in a way that is consistent with the evidence for the involvement of the hippocampus in more general forms of memory.A key anatomical feature of area CA3 is that its pyramidal cells receive the majority of their inputs from other CA3 pyramidal cells (Amaral and Witter, 1989;Amaral et al., 1990). The resulting recurrent network has been extensively explored as a plastic attractor model of the way that the hippocampus acts as a general memory (Marr, 1971;McNaughton and Morris, 1987;Hasselmo et al., 1996;Levy, 1996;Rolls, 1996) but has been widely ignored by models that are intended to account for various properties of place cells (Zipser, 1985;Sharp, 1991;Touretzky and Redish, 1996; Burgess et al., 1997) (but see Battaglia and Treves, 1998).The model of Samsonovich and McN...