Abstract
Mitral and tufted cells (MTCs) of the mammalian olfactory bulb are connected via dendrodendritic synapses with inhibitory interneurons in the external plexiform layer. The range, spatial layout, and temporal properties of inhibitory interactions between MTCs mediated by inhibitory interneurons remain unclear. Therefore, we tested for inhibitory interactions using an optogenetic approach. We optically stimulated MTCs expressing channelrhodopsin-2 in transgenic mice, while recording from individual MTCs in juxtacellular or whole-cell configuration in vivo. We used a spatial noise stimulus for mapping interactions between MTCs belonging to different glomeruli in the dorsal bulb. Analyzing firing responses of MTCs to the stimulus, we did not find robust lateral inhibitory effects that were spatially specific. However, analysis of sub-threshold changes in the membrane potential revealed evidence for inhibitory interactions between MTCs that belong to different glomerular units. These lateral inhibitory effects were short-lived and spatially specific. MTC response maps showed hyperpolarizing effects radially extending over more than five glomerular diameters. The inhibitory maps exhibited non-symmetrical yet distance-dependent characteristics.
Highlights
Neurons in sensory systems are often spatially arranged such that cells responding to similar stimuli cluster in functional or even morphologically defined modules
By direct stimulation of mitral and tufted cells (MTCs) we focused our observations on effects mediated in the external plexiform layer (EPL) by inhibitory interneurons, since we most likely omitted the lateral inhibitory effects that occur in the glomerular layer after sensory input via olfactory sensory neurons (OSNs) (Shepherd et al, 2004; Fukunaga et al, 2014)
We asked if it is possible to record from a given MTC and map the location of its parent glomerulus by illuminating the dorsal olfactory bulb (OB) using binary white noise stimuli with 50 Hz frame transitions (Figures 1A,B)
Summary
Neurons in sensory systems are often spatially arranged such that cells responding to similar stimuli cluster in functional or even morphologically defined modules. In the mammalian olfactory bulb (OB) this modular organization is governed by the convergence of axons from olfactory sensory neurons (OSNs) expressing the same receptor type onto the same functional unit, the glomeruli (Mombaerts et al, 1996). Principal OB neurons, the mitral and tufted cells (MTCs), primarily receive sensory input through a single apical dendrite ramifying in only one glomerulus, and they project their axons via the lateral olfactory tract (LOT) to the olfactory cortex (Shepherd et al, 2004). Lateral interaction between neurons responding to similar stimuli is a general mechanism for contrast enhancement and optimization of sensory representations (Giridhar et al, 2011; Isaacson and Scanziani, 2011). It could serve to de-correlate stimulus representations (Friedrich and Laurent, 2001) and improve olfactory discrimination performance (Abraham et al, 2010).
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