Canonical Organization of Layer 1 Neuron-Led Cortical Inhibitory and Disinhibitory Interneuronal Circuits

Abstract

Interneurons play a key role in cortical function and dysfunction, yet organization of cortical interneuronal circuitry remains poorly understood. Cortical Layer 1 (L1) contains 2 general GABAergic interneuron groups, namely single bouquet cells (SBCs) and elongated neurogliaform cells (ENGCs). SBCs predominantly make unidirectional inhibitory connections (SBC→) with L2/3 interneurons, whereas ENGCs frequently form reciprocal inhibitory and electric connections (ENGC↔) with L2/3 interneurons. Here, we describe a systematic investigation of the pyramidal neuron targets of L1 neuron-led interneuronal circuits in the rat barrel cortex with simultaneous octuple whole-cell recordings and report a simple organizational scheme of the interneuronal circuits. Both SBCs→ and ENGC ↔ L2/3 interneuronal circuits connect to L2/3 and L5, but not L6, pyramidal neurons. SBC → L2/3 interneuronal circuits primarily inhibit the entire dendritic-somato-axonal axis of a few L2/3 and L5 pyramidal neurons located within the same column. In contrast, ENGC ↔ L2/3 interneuronal circuits generally inhibit the distal apical dendrite of many L2/3 and L5 pyramidal neurons across multiple columns. Finally, L1 interneuron-led circuits target distinct subcellular compartments of L2/3 and L5 pyramidal neurons in a L2/3 interneuron type-dependent manner. These results suggest that L1 neurons form canonical interneuronal circuits to control information processes in both supra- and infragranular cortical layers.

The roadmap for estimation of cell-type-specific neuronal activity from non-invasive measurements

“…Fortunately, synaptic projections (i.e. projection 'domains') from at least some types of inhibitory neurons onto PCs segregate along the depth axis (figure 7c) [143,152]. For example, somatostatin-positive Martinotti cells synapse on the apical dendrites [153] while double bouquet cells positive for neuronal nitric oxide synthase synapse at the basal dendrites [143].…”

Synaptic Microcircuits in the Barrel Cortex

“…All L2/3 interneurons studied by Jiang et al [186] and Lee et al [187] project onto L2, L3, L5A and L5B pyramidal cells but apparently not L6 pyramidal cells. However, they target different cellular compartments (see Fig.…”

“…Two recent and very detailed studies [186,187] (see below) described the disynaptic interaction between L1 interneurons and L2/3 interneuron types.The authors of this work also investigated synaptic connections established between different L2/3 interneuron types and pyramidal cells in layers 2/3 and 5. Several distinct L2/3 interneuron types were identified: Martinotti cells, chandelier cells, NGFCs, double bouquet cells (DBCs), bitufted cells (BTCs), bipolar cells (BPCs), as well as BCs (Fig.…”

CaV3.2 calcium channels control NMDA receptor-mediated transmission: a new mechanism for absence epilepsy

“…Using our recently developed stable multiple patch clamp recording system (Jiang et al 2013;Lee et al 2014b;Wang et al 2015), simultaneous and/or sequential multiple whole-cell recordings were obtained from two to five nearby infected and noninfected TRN neurons or cortical L5 or hippocampal CA1 pyramidal neurons under visual guidance using fluorescence and transmitted light illumination. For cultured slices, bath solution (29°C ± 1.5°C) contained 119 mM NaCl, 2.5 mM KCl, 4 mM CaCl 2 , 4 mM MgCl 2 , 26 mM NaHCO 3 , 1 mM NaH 2 PO 4 , 11 mM glucose, 0.1 mM picrotoxin (PTX), 0.01 mM bicuculline, and 0.002 mM 2-chloroadenosine (pH 7.4) gassed with 5% CO 2 /95% O 2 .…”