The presubiculum contains head direction cells that are crucial for spatial orientation. Here, we examined the connectivity and strengths of thalamic inputs to presubicular layer 3 neurons projecting to the medial entorhinal cortex in the mouse. We recorded pairs of projection neurons and interneurons while optogenetically stimulating afferent fibers from the anterior thalamic nuclei. Thalamic input differentially affects presubicular neurons: layer 3 pyramidal neurons and fast-spiking parvalbumin-expressing interneurons are directly and monosynaptically activated, with depressing dynamics, whereas somatostatin-expressing interneurons are indirectly excited, during repetitive anterior thalamic nuclei activity. This arrangement ensures that the thalamic excitation of layer 3 cells is often followed by disynaptic inhibition. Feedforward inhibition is largely mediated by parvalbumin interneurons, which have a high probability of connection to presubicular pyramidal cells, and it may enforce temporally precise head direction tuning during head turns. Our data point to the potential contribution of presubicular microcircuits for fine-tuning thalamic head direction signals transmitted to medial entorhinal cortex.SIGNIFICANCE STATEMENT How microcircuits participate in shaping neural inputs is crucial to understanding information processing in the brain. Here, we show how the presubiculum may process thalamic head directional information before transmitting it to the medial entorhinal cortex. Synaptic inputs from the anterior thalamic nuclei excite layer 3 pyramidal cells and parvalbumin interneurons, which mediate disynaptic feedforward inhibition. Somatostatin interneurons are excited indirectly. Presubicular circuits may switch between two regimens depending on the angular velocity of head movements. During immobility, somatostatin-pyramidal cell interactions could support maintained head directional firing with attractor-like dynamics. During rapid head turns, in contrast, parvalbumin-mediated feedforward inhibition may act to tune the head direction signal transmitted to medial entorhinal cortex.

The subiculum is the major output structure of the hippocampal formation and is involved in learning and memory as well as in spatial navigation. Little is known about how neuronal diversity contributes to function in the subiculum. Previously, in vitro studies have identified distinct bursting patterns in the subiculum. Here, we asked how burst firing is related to spatial coding in vivo Using juxtacellular recordings in freely moving male rats, we studied the bursting behavior of 102 subicular principal neurons and distinguished two populations: sparsely bursting (∼80%) and dominantly bursting neurons (∼20%). These bursting behaviors were not linked to anatomy: both cell types were found all along the proximodistal and radial axes of the subiculum and all identified cells were pyramidal neurons. However, the distinct burst firing patterns were related to functional differences: the activity of sparsely bursting cells showed a stronger spatial modulation than the activity of dominantly bursting neurons. In addition, all cells classified as boundary cells were sparsely bursting cells. In most sparsely bursting cells, bursts defined sharper firing fields and carried more spatial information than isolated spikes. We conclude that burst firing is functionally relevant to subicular spatially tuned neurons, possibly by serving as a mechanism to transmit spatial information to downstream structures.SIGNIFICANCE STATEMENT The subiculum is the major output structure of the hippocampal formation and is involved in spatial navigation. In vitro, subicular cells can be distinguished by their ability to initiate bursts as brief sequences of spikes fired at high frequencies. Little is known about the relationship between cellular diversity and spatial coding in the subiculum. We performed high-resolution juxtacellular recordings in freely moving rats and found that bursting behavior predicts functional differences between subicular neurons. Specifically, sparsely bursting cells have lower firing rates and carry more spatial information than dominantly bursting cells. Additionally, bursts fired by sparsely bursting cells encoded spatial information better than isolated spikes, indicating that bursts act as a unit of information dedicated to spatial coding.