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J Neurosci. 2018 Jul 11;38(28):6411-6425. doi: 10.1523/JNEUROSCI.0014-18.2018. Epub 2018 Jun 19.

Anterior Thalamic Excitation and Feedforward Inhibition of Presubicular Neurons Projecting to Medial Entorhinal Cortex.

Author information

1
Institut National de la Santé et de la Recherche Médicale U1127, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7225, Sorbonne Universités, UPMC Université Paris 6, Unité Mixte de Recherche S1127, Institut du Cerveau et de la Moelle épinière, 75013 Paris, France.
2
Centre National de la Recherche Scientifique Unité Mixte de Recherche 8119, Université Paris Descartes, 75006 Paris, France.
3
Institut National de la Santé et de la Recherche Médicale U1130, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246, UPMC Neuroscience Paris Seine, 75005 Paris, France.
4
Institut of Occupational, Social and Environmental Medicine, Goethe University, 60590 Frankfurt, Germany, and.
5
Institut National de la Santé et de la Recherche Médicale U1127, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7225, Sorbonne Universités, UPMC Université Paris 6, Unité Mixte de Recherche S1127, Institut du Cerveau et de la Moelle épinière, 75013 Paris, France, desdemona.fricker@parisdescartes.fr.

Abstract

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.

KEYWORDS:

head direction; hippocampus; interneurons; optogenetics; patch clamp; postsubiculum

PMID:
29921712
PMCID:
PMC6231540
[Available on 2019-01-11]
DOI:
10.1523/JNEUROSCI.0014-18.2018

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