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Inhibition Among Olfactory Receptor Neurons View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Frontiers - Publisher Connector MINI REVIEW ARTICLE published: 23 October 2013 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2013.00690 Inhibition among olfactory receptor neurons Wynand Van der Goes van Naters* School of Biosciences, Cardiff University, Cardiff, UK Edited by: Often assumed to be epiphenomena of a cell’s activity, extracellular currents and resulting Shennan A. Weiss, Columbia potential changes are increasingly recognized to influence the function of other cells in the University, USA vicinity. Experimental evidence shows that even small electric fields can modulate spike Reviewed by: timing in neurons. Moreover, when neurons are brought close together experimentally Alberto E. Pereda, Albert Einstein College of Medicine of Yeshiva or in pathological conditions, activity in one neuron can excite its neighbors. Inhibitory University, USA ephaptic mechanisms, however, may depend on more specialized coupling among cells. Theresa M. Szabo-Maas, Delaware Recent studies in the Drosophila olfactory system have shown that excitation of a State University, USA sensory neuron can inhibit its neighbor, and it was speculated that this interaction was *Correspondence: ephaptic. Here we give an overview of ephaptic interactions that effect changes in spike Wynand Van der Goes van Naters, School of Biosciences, Cardiff timing, excitation or inhibition in diverse systems with potential relevance to human University, Museum Avenue, neuroscience. We examine the mechanism of the inhibitory interaction in the Drosophila CF10 3AX Cardiff, UK system and that of the well-studied ephaptic inhibition of the Mauthner cell in more e-mail: vandergoesvannaterswm@ detail. We note that both current towards and current away from the local extracellular cardiff.ac.uk environment of a neuron can inhibit it, but the mechanism depends on the specific architecture of each system. Keywords: olfaction, inhibition, ephaptic, sensillum, sensory neurons, Drosophila While chemical and electrical synapses are anatomically the cell can change local Ve and thereby Vm.Thedirectionof identifiable specialized contacts that mediate interactions electric current is defined arbitrarily as if only positive charges among cells, electric fields and currents produced by cells in aremoving,sointhecaseofmovementofanionsthecurrent their local environment may also influence the activity of their is opposite in direction to the actual anionic flow. Current flow neighbors (Jefferys, 1995; Anastassiou et al., 2011). The extent to the local extracellular environment may hyperpolarize the to which these ephaptic interactions contribute to information membrane by making Ve more positive, while current flow away processing in the human nervous system is not yet clear. Our may reduce the absolute potential difference between Vi and Ve. understanding of ephaptic mechanisms has been especially Current flow is the result of an electric field, which is defined as informed by investigating the communication among cells in theforceperunitpositivechargeactingonachargedparticleand several very tractable systems, including the Mauthner cells in fish is expressed in newtons per coulomb or volts per meter (N/C = (Furukawa and Furshpan, 1963;reviewedinZottoli and Faber, V/m). A field can act to drive current in the extracellular space 2000; Korn and Faber, 2005; Weiss and Faber, 2010). Recently, Su and also across the membrane and intracellularly. et al. (2012) showed that inhibitory interactions among grouped Even very small fields can change the timing of spikes gener- olfactory sensory neurons in the fruit fly Drosophila melanogaster ated by neurons, as was shown in rat cortical pyramidal neurons modulate their responses to odors, suggesting that processing where changes under 0.2 mV in Ve induced by an external of olfactory information may already begin among neurons oscillating field could entrain spikes (Anastassiou et al., 2011). within the sensory organs. Blocking synaptic transmission by Small electric fields, when concurrent to other suprathreshold several experimental means did not remove the inhibition, which input, also had significant effects in rat hippocampal neurons on together with other considerations led the authors to hypothesize spike timing and these could be magnified by dynamic network that an ephaptic mechanism underlies the interaction. Here activity (Radman et al., 2007; Reato et al., 2010). It is becoming we present a brief overview of ephaptic interactions in diverse increasingly clear that, in addition to the firing rate of an individ- systems and then focus on inhibitory ephaptic mechanisms in the ual neuron, its precise spike timing in an ensemble of neurons in Mauthner cell system and in the Drosophila olfactory system. a circuit has an important role in relaying information (De Zeeuw The transmembrane potential (Vm) of a cell is the difference et al., 2011). Moreover, the degree of phase-locking of hippocam- between the electrical potential inside the cell (Vi)andthepoten- pal neurons to the theta-oscillation was shown to be predictive tial externally (Ve), which are both measured against the same for the strength of human memory formation (Rutishauser et al., (distant) reference point, such that Vm = Vi−Ve. The resting 2010), indicating a role for spike timing in information storage. Vm in many neurons is approximately −70 mV. While Ve is often The ability of electric fields to affect spike timing suggests ephaptic assumed to be constant and assigned a value of 0 V by convention, interactions may indeed contribute to information processing in current flow to or from the local extracellular environment near the brain in combination with other intercellular mechanisms. Frontiers in Human Neuroscience www.frontiersin.org October 2013 | Volume 7 | Article 690 | 1 Van der Goes van Naters Ephaptic inhibition in olfaction Ephaptic effects on spike timing may also play a role in the through interneurons limits activation of the Mauthner cell to a pathological transition from synchronous discharge into epileptic single spike and stops simultaneous excitation of the other Mau- seizure in several brain areas (Jefferys, 1995; Vigmond et al., 1997; thner cell, which together results in the characteristic C-shaped McCormick and Contreras, 2001). whipping movement of the body that displaces the animal away In addition to modulating the timing of spikes, stronger fields from the triggering stimuli. The fast inhibition arrives at the same can bring neurons to threshold, especially under experimental time as the Mauthner cell receives excitatory input, suggesting that or pathological conditions. Indeed, early studies showed that the inhibition contributes to setting the threshold of the startle action potentials could be transmitted between two experimen- response (Weiss et al., 2008). An ephaptic mechanism underlies tally apposed squid giant axon fibers (Arvanitaki, 1942; Ramón, the fast inhibition (Furukawa and Furshpan, 1963). The axons of and Moore, 1978)anditwasArvanitaki (1942) who first called specific interneurons terminate near the axon hillock of the Mau- the zone of contact or close vicinity, where the cells can influ- thner cell in a highly organized structure, the axon cap. The axon ence each other’s activity, an ephapse. Clinically, the sudden terminals are unmyelinated and, on excitation of the interneu- sharp pains experienced by patients with trigeminal neuralgia rons, inward currents at the last node of Ranvier cause current may in part be caused by ephaptic neurotransmission between to flow out from the axon terminals into the local environment apposed denuded axonal membranes of nociceptors near the of the Mauthner cell. High electrical resistance in the axon cap trigeminal ganglion (Oaklander, 2008). Similarly, the involuntary causes the current flow into it to locally increase Ve around part of contractions of facial muscles in hemi-facial spasm have been the Mauthner cell. While leakage across the Mauthner membrane attributed to ephapsis among fibers in the facial nerve when it is also causes a slight increase in Vi, simultaneous measurements chronically but often subclinically injured by pressure of a blood of Ve and Vi have shown that the increase in Ve is much larger vessel, although mechanisms such as ectopic generation of muscle suggesting that the potential increase is indeed due to current discharges may also contribute (Valls-Solé, 2013). Computational from an extrinsic source. In the Mauthner system, a current from approaches suggest that close apposition, as occurs among the the axon terminals of interneurons to the environment around tightly packed fascicles of unmyelinated axons of olfactory recep- part of the Mauthner cell thereby results in a local extrinsic tor neurons, also allows an action potential in one fiber to elicit hyperpolarizing potential (EHP) that inhibits the cell’s activity. action potentials in its neighbors under normal physiological con- Reciprocal ephaptic inhibition also occurs. An action potential ditions through ephaptic coupling (Bokil et al., 2001), so even in in the Mauthner cell leads to a passive hyperpolarizing potential the absence of gap junctions between them (Blinder et al., 2003). (PHP) in the interneurons innervating the axon cap, which has In contrast to excitatory coupling, ephaptic inhibition among been used experimentally to identify them, because the action cells may require specialized anatomical, molecular and electrical current leaves
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