Abstract
Martinotti cells are the most prominent distal dendrite–targeting interneurons in the cortex, but their role in controlling pyramidal cell (PC) activity is largely unknown. Here, we show that the nicotinic acetylcholine receptor α2 subunit (Chrna2) specifically marks layer 5 (L5) Martinotti cells projecting to layer 1. Furthermore, we confirm that Chrna2-expressing Martinotti cells selectively target L5 thick-tufted type A PCs but not thin-tufted type B PCs. Using optogenetic activation and inhibition, we demonstrate how Chrna2-Martinotti cells robustly reset and synchronize type A PCs via slow rhythmic burst activity and rebound excitation. Moreover, using optical feedback inhibition, in which PC spikes controlled the firing of surrounding Chrna2-Martinotti cells, we found that neighboring PC spike trains became synchronized by Martinotti cell inhibition. Together, our results show that L5 Martinotti cells participate in defined cortical circuits and can synchronize PCs in a frequency-dependent manner. These findings suggest that Martinotti cells are pivotal for coordinated PC activity, which is involved in cortical information processing and cognitive control.
Highlights
Martinotti cells, ubiquitous to the cortex [1], are the most prominent cross-laminar interneuron subtype forming synapses in layer 1 onto the distal dendrites of cortical pyramidal cells (PCs) [1,2,3]
Out of 37 (97.3%) cells met the criteria of deep layer Martinotti cells by having an ovoid cell body in layer 5 (L5), bipolar dendritic morphology, axons emerging from the main dendrite, proximal axonal arborizations, and long axonal projections to layer 1 with a dense arborization around
Voltage clamp experiments further highlighted the presence of large IPSCs in type A PCs (107.40 ± 3.54 pA, n = 3 cells; Fig 4E, top, S4 Data) and the absence of IPSCs in type B PCs (n = 3 cells; Fig 4E, bottom). These results show that a rapid burst of MCα2 action potential (AP) can abruptly halt the firing of type A PCs and reset PC firing by temporal coupling rebound APs of PCs while leaving type B PC firing unaffected
Summary
Martinotti cells, ubiquitous to the cortex [1], are the most prominent cross-laminar interneuron subtype forming synapses in layer 1 onto the distal dendrites of cortical pyramidal cells (PCs) [1,2,3]. Despite this close structural relationship, the role of Martinotti cell inhibition is not clear. Studies identifying Martinotti cells by various markers have found different morphologies and microcircuit connectivity depending on the cortical layer in which their cell bodies reside [2]. SOM+ Martinotti cells are often referred to as low-threshold spiking (LTS) neurons [3] or slow-inhibitory interneurons [11], early studies have shown up to four different firing patterns for Martinotti cells [2,9]
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