Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum.
The presubiculum is part of the parahippocampal spatial navigation system and contains head direction and grid cells upstream of the medial entorhinal cortex. This position within the parahippocampal cortex renders the presubiculum uniquely suited for analyzing the circuit requirements underlying the emergence of spatially tuned neuronal activity. To identify the local circuit properties, we analyzed the topology of synaptic connections between pyramidal cells and interneurons in all layers of the presubiculum by testing 4250 potential synaptic connections using multiple whole-cell recordings of up to 8 cells simultaneously. Network topology showed layer-specific organization of microcircuits consistent with the prevailing distinction of superficial and deep layers. While connections among pyramidal cells were almost absent in superficial layers, deep layers exhibited an excitatory connectivity of 3.9%. In contrast, synaptic connectivity for inhibition was higher in superficial layers though markedly lower than in other cortical areas. Finally, synaptic amplitudes of both excitatory and inhibitory connections showed log-normal distributions suggesting a nonrandom functional connectivity. In summary, our study provides new insights into the microcircuit organization of the presubiculum by revealing area- and layer-specific connectivity rules and sets new constraints for future models of the parahippocampal navigation system.
Institute of Neurophysiology, Charité - Universitätsmedizin, 10117 Berlin, Germany.
Yangfan
Y
Peng
Institute for Integrative Neuroanatomy, Charité - Universitätsmedizin, 10117 Berlin, Germany.
Federico J
FJ
Barreda Tomás
Institute of Neurophysiology, Charité - Universitätsmedizin, 10117 Berlin, Germany.
Constantin
C
Klisch
Institute for Integrative Neuroanatomy, Charité - Universitätsmedizin, 10117 Berlin, Germany.|NeuroCure Cluster of Excellence, Charité - Universitätsmedizin, 10117 Berlin, Germany.
Imre
I
Vida
Institute of Neurophysiology, Charité - Universitätsmedizin, 10117 Berlin, Germany.|NeuroCure Cluster of Excellence, Charité - Universitätsmedizin, 10117 Berlin, Germany.
Jörg R P
JRP
Geiger
D000818:Animals; D001931:Brain Mapping; D007150:Immunohistochemistry; D007395:Interneurons / Q000166:cytology* / Q000502:physiology; D009434:Neural Pathways / Q000166:cytology* / Q000502:physiology; D020534:Parahippocampal Gyrus / Q000166:cytology* / Q000502:physiology; D018408:Patch-Clamp Techniques; D051381:Rats; D055647:Rats, Transgenic; D017208:Rats, Wistar; D065854:Spatial Navigation / Q000502:physiology*; D013569:Synapses / Q000502:physiology*
grid cells; head direction cells; log-normal; multipatch recording; network topology