Efficient phase coding in hippocampal place cells

Abstract

Hippocampal place cells encode space through phase precession, whereby neuronal spike phase progressively advances during place-field traversals. What neural constraints are essential for achieving efficient transfer of information through such phase codes, while concomitantly maintaining signature neuronal excitability specific to individual cell types? We developed a conductance-based model for phase precession in CA1 pyramidal neurons within the temporal sequence compression framework, and defined phase-coding efficiency using information theory. We recruited an unbiased stochastic search strategy to build a model population that exhibited physiologically observed heterogeneities in intrinsic properties. Place-field responses elicited from these models matched signature sub- and supra-threshold place-cell characteristics, including phase precession, sub-threshold voltage ramps, increases in theta-frequency power and firing rate during place-field traversals. Employing this model population, we show that disparate parametric combinations with weak pair-wise correlations resulted in models with similar high-efficiency phase codes and similar excitability characteristics. Mechanistically, the emergence of such parametric degeneracy was dependent on the differential and variable impact of individual ion channels on phase-coding efficiency in different models, and importantly, on synergistic interactions between synaptic and intrinsic properties. Furthermore, our analyses predicted a dominant role for calcium-activated potassium channels in regulating phase precession and coding efficiency. Finally, change in afferent statistics, manifesting as input asymmetry, induced an adaptive shift in the phase code that preserved its efficiency, apart from introducing asymmetry in sub-threshold ramps and firing profiles during place-field traversals. Our study postulates degeneracy as a potential framework to attain the twin goals of efficient temporal coding and robust homeostasis. SIGNIFICANCE STATEMENT Neuronal intrinsic properties exhibit significant baseline heterogeneities, and change with activity-dependent plasticity and neuromodulation. How do hippocampal neurons encode spatial locations through the precise timings of their action potentials in the face of such heterogeneities? Here, employing a unifying synthesis of the temporal sequence compression, efficient coding and degeneracy frameworks, we show that there are several disparate routes for neurons to achieve high-efficiency spatial information transfer through such temporal codes. These disparate routes were consequent to the ability of neurons to produce precise encoding through distinct structural components, critically involving synergistic interactions between intrinsic and synaptic properties. Our results point to an explosion in the degrees of freedom available to a neuron in concomitantly achieving efficient coding and excitability homeostasis.