Pyramidal Cell-Interneuron Circuit Architecture and Dynamics in Hippocampal Networks.

Excitatory control of inhibitory neurons is poorly understood due to the difficulty of studying synaptic connectivity in vivo. We inferred such connectivity through analysis of spike timing and validated this inference using juxtacellular and optogenetic control of presynaptic spikes in behaving mice. We observed that neighboring CA1 neurons had stronger connections and that superficial pyramidal cells projected more to deep interneurons. Connection probability and strength were skewed, with a minority of highly connected hubs. Divergent presynaptic connections led to synchrony between interneurons. Synchrony of convergent presynaptic inputs boosted postsynaptic drive. Presynaptic firing frequency was read out by postsynaptic neurons through short-term depression and facilitation, with individual pyramidal cells and interneurons displaying a diversity of spike transmission filters. Additionally, spike transmission was strongly modulated by prior spike timing of the postsynaptic cell. These results bridge anatomical structure with physiological function.

How environment and self-motion combine in neural representations of space.

Estimates of location or orientation can be constructed solely from sensory information representing environmental cues. In unfamiliar or sensory-poor environments, these estimates can also be maintained and updated by integrating self-motion information. However, the accumulation of error dictates that updated representations of heading direction and location become progressively less reliable over time, and must be corrected by environmental sensory inputs when available. Anatomical, electrophysiological and behavioural evidence indicates that angular and translational path integration contributes to the firing of head direction cells and grid cells. We discuss how sensory inputs may be combined with self-motion information in the firing patterns of these cells. For head direction cells, direct projections from egocentric sensory representations of distal cues can help to correct cumulative errors. Grid cells may benefit from sensory inputs via boundary vector cells and place cells. However, the allocentric code of boundary vector cells and place cells requires consistent head-direction information in order to translate the sensory signal of egocentric boundary distance into allocentric boundary vector cell firing, suggesting that the different spatial representations found in and around the hippocampal formation are interdependent. We conclude that, rather than representing pure path integration, the firing of head-direction cells and grid cells reflects the interface between self-motion and environmental sensory information. Together with place cells and boundary vector cells they can support a coherent unitary representation of space based on both environmental sensory inputs and path integration signals.