Anatomical Organization and Spatiotemporal Firing Patterns of Layer 3 Neurons in the Rat Medial Entorhinal Cortex.
Layer 3 of the medial entorhinal cortex is a major gateway from the neocortex to the hippocampus. Here we addressed structure-function relationships in medial entorhinal cortex layer 3 by combining anatomical analysis with juxtacellular identification of single neurons in freely behaving rats. Anatomically, layer 3 appears as a relatively homogeneous cell sheet. Dual-retrograde neuronal tracing experiments indicate a large overlap between layer 3 pyramidal populations, which project to ipsilateral hippocampus, and the contralateral medial entorhinal cortex. These cells were intermingled within layer 3, and had similar morphological and intrinsic electrophysiological properties. Dendritic trees of layer 3 neurons largely avoided the calbindin-positive patches in layer 2. Identification of layer 3 neurons during spatial exploration (n = 17) and extracellular recordings (n = 52) pointed to homogeneous spatial discharge patterns. Layer 3 neurons showed only weak spiking theta rhythmicity and sparse head-direction selectivity. A majority of cells (50 of 69) showed no significant spatial modulation. All of the ∼28% of neurons that carried significant amounts of spatial information (19 of 69) discharged in irregular spatial patterns. Thus, layer 3 spatiotemporal firing properties are remarkably different from those of layer 2, where theta rhythmicity is prominent and spatially modulated cells often discharge in grid or border patterns. Significance statement: Neurons within the superficial layers of the medial entorhinal cortex (MEC) often discharge in border, head-direction, and theta-modulated grid patterns. It is still largely unknown how defined discharge patterns relate to cellular diversity in the superficial layers of the MEC. In the present study, we addressed this issue by combining anatomical analysis with juxtacellular identification of single layer 3 neurons in freely behaving rats. We provide evidence that the anatomical organization and spatiotemporal firing properties of layer 3 neurons are remarkably different from those in layer 2. Specifically, most layer 3 neurons discharged in spatially irregular firing patterns, with weak theta-modulation and head-directional selectivity. This work thus poses constraints on the spatiotemporal patterns reaching downstream targets, like the hippocampus.
Bernstein Center for Computational Neuroscience.
Qiusong
Q
Tang
Bernstein Center for Computational Neuroscience, Berlin School of Mind and Brain, Humboldt University of Berlin, 10115 Berlin, Germany.
Christian Laut
CL
Ebbesen
Bernstein Center for Computational Neuroscience.
Juan Ignacio
JI
Sanguinetti-Scheck
Werner-Reichardt Centre for Integrative Neuroscience, University of Tübingen, 72076 Tübingen, Germany, and.
Patricia
P
Preston-Ferrer
Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.
Anja
A
Gundlfinger
Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.
Jochen
J
Winterer
Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.
Prateep
P
Beed
Bernstein Center for Computational Neuroscience.
Saikat
S
Ray
Bernstein Center for Computational Neuroscience.
Robert
R
Naumann
Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.
Dietmar
D
Schmitz
Bernstein Center for Computational Neuroscience, andrea.burgalossi@cin.uni-tuebingen.de michael.brecht@bccn-berlin.de.
Michael
M
Brecht
Werner-Reichardt Centre for Integrative Neuroscience, University of Tübingen, 72076 Tübingen, Germany, and andrea.burgalossi@cin.uni-tuebingen.de michael.brecht@bccn-berlin.de.
Andrea
A
Burgalossi
D000200:Action Potentials; D000818:Animals; D064026:Calbindins / Q000235:genetics / Q000378:metabolism; D018728:Entorhinal Cortex / Q000166:cytology / Q000502:physiology*; D017966:Pyramidal Cells / Q000378:metabolism / Q000502:physiology*; D051381:Rats; D017208:Rats, Wistar; D013826:Theta Rhythm
D064026:Calbindins
head-direction cell; juxtacellular recordings; layer 3; medial entorhinal cortex; spatial navigation