Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat.
Whole-cell patch-clamp recordings followed by histochemical staining and single-cell RT-PCR were obtained from 180 Martinotti interneurones located in layers II to VI of the somatosensory cortex of Wistar rats (P13-P16) in order to examine their anatomical, electrophysiological and molecular properties. Martinotti cells (MCs) mostly displayed ovoid-shaped somata, bitufted dendritic morphologies, and axons with characteristic spiny boutons projecting to layer I and spreading horizontally across neighbouring columns more than 1 mm. Electron microscopic examination of MC boutons revealed that all synapses were symmetrical and most synapses (71%) were formed onto dendritic shafts. MCs were found to contact tuft, apical and basal dendrites in multiple neocortical layers: layer II/III MCs targeted mostly layer I and to a lesser degree layer II/III; layer IV MCs targeted mostly layer IV and to a lesser degree layer I; layer V and VI MCs targeted mostly layer IV and layer I and to a lesser degree the layer in which their somata was located. MCs typically displayed spike train accommodation (90%; n = 127) in response to depolarizing somatic current injections, but some displayed non-accommodating (8%) and a few displayed irregular spiking responses (2%). Some accommodating and irregular spiking MCs also responded initially with bursts (17%). Accommodating responses were found in all layers, non-accommodating mostly in upper layers and bursting mostly in layer V. Single-cell multiplex RT-PCR performed on 63 MCs located throughout layers II-VI, revealed that all MCs were somatostatin (SOM) positive, and negative for parvalbumin (PV) as well as vasoactive intestinal peptide (VIP). Calbindin (CB), calretinin (CR), neuropeptide Y (NPY) and cholecystokinin (CCK) were co- expressed with SOM in some MCs. Some layer-specific trends seem to exist. Finally, 24 accommodating MCs were examined for the expression of 26 ion channel genes. The ion channels with the highest expression in these MCs were (from highest to lowest); Cabeta1, Kv3.3, HCN4, Cabeta4, Kv3.2, Kv3.1, Kv2.1, HCN3, Caalpha1G, Kv3.4, Kv4.2, Kv1.1 and HCN2. In summary, this study provides the first detailed analysis of the anatomical, electrophysiological and molecular properties of Martinotti cells located in different neocortical layers. It is proposed that MCs are crucial interneurones for feedback inhibition in and between neocortical layers and columns.
Wang
Yun
Y
Division of Neurology Research, St. Elizabeth's Medical Center, Tufts University, Boston, MA 02135, USA.
Toledo-Rodriguez
Maria
M
Gupta
Anirudh
A
Wu
Caizhi
C
Silberberg
Gilad
G
Luo
Junyi
J
Markram
Henry
H
D000200:Action Potentials / Q000502:physiology; D000367:Age Factors; D000818:Animals; D048430:Cell Shape / Q000502:physiology; D020869:Gene Expression Profiling; D007395:Interneurons / Q000166:cytology* / Q000502:physiology*; D007473:Ion Channels / Q000235:genetics; D009479:Neuropeptides / Q000235:genetics; D018408:Patch-Clamp Techniques; D051381:Rats; D017208:Rats, Wistar; D013003:Somatosensory Cortex / Q000166:cytology* / Q000502:physiology*; D013569:Synapses / Q000502:physiology
D007473:Ion Channels; D009479:Neuropeptides