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Spikelets in Pyramidal Neurons Rev. Neurosci. 2020; 31(1): 101–119 Martina Michalikova, Michiel W.H. Remme, Dietmar Schmitz, Susanne Schreiber and Richard Kempter* Spikelets in pyramidal neurons: generating mechanisms, distinguishing properties, and functional implications https://doi.org/10.1515/revneuro-2019-0044 the various mechanisms that can give rise to spikelets. Received April 8, 2019; accepted May 13, 2019; previously published For each mechanism, we present the biophysical under- online August 22, 2019 pinnings as well as the resulting properties of spikelets and compare these predictions to experimental data from Abstract: Spikelets are small spike-like depolarizations pyramidal neurons. We also discuss the functional impli- that are found in somatic recordings of many neuron cations of each mechanism. On the example of pyramidal types. Spikelets have been assigned important functions, neurons, we illustrate that several independent spikelet- ranging from neuronal synchronization to the regulation generating mechanisms fulfilling vastly different func- of synaptic plasticity, which are specific to the particular tions might be operating in a single cell. mechanism of spikelet generation. As spikelets reflect spiking activity in neuronal compartments that are elec- Keywords: action potential initiation; axon initial segment; trotonically distinct from the soma, four modes of spike- dendritic spikes; ephaptic coupling; gap junction. let generation can be envisaged: (1) dendritic spikes or (2) axonal action potentials occurring in a single cell as well as action potentials transmitted via (3) gap junctions or Introduction (4) ephaptic coupling in pairs of neurons. In one of the best studied neuron type, cortical pyramidal neurons, Spikelets are non-synaptic events of small amplitudes the origins and functions of spikelets are still unresolved; (<30 mV) that are observed in intracellular record- all four potential mechanisms have been proposed, but ings of many types of neurons (e.g. in thalamocortical the experimental evidence remains ambiguous. Here we neurons, Hughes et al., 2002; thalamic reticular neurons, attempt to reconcile the scattered experimental findings Fuentealba et al., 2004; hippocampal interneurons, in a coherent theoretical framework. We review in detail Zhang et al., 2004). Because of their spike-like appear- ance and all-or-none character, spikelets are considered *Corresponding author: Richard Kempter, Institute for Theoretical to originate in action potentials (APs) generated in elec- Biology, Department of Biology, Humboldt-Universität zu Berlin, trotonically distinct neuronal compartments, when cur- D-10115 Berlin, Germany; Bernstein Center for Computational rents from a remote AP influence the membrane voltage of Neuroscience Berlin, Philippstr. 13, D-10115 Berlin, Germany; and the recorded compartment but do not suffice to initiate an Einstein Center for Neurosciences Berlin, D-10117 Berlin, Germany, AP there. As spikelets are typically measured in somatic e-mail: [email protected] Martina Michalikova and Michiel W.H. Remme: Institute for recordings, the underlying APs might, in principle, occur Theoretical Biology, Department of Biology, Humboldt-Universität zu in dendritic or axonal compartments within the same cell Berlin, D-10115 Berlin, Germany or in another cell coupled by gap junctions or ephaptically Dietmar Schmitz: Neuroscience Research Center, Charite- through extracellular fields (Figure 1). University Medicine, D-10117 Berlin, Germany; Bernstein Center As each of these mechanisms has different functional for Computational Neuroscience Berlin, D-10115 Berlin, Germany; implications, it is important to determine the origin of Einstein Center for Neurosciences Berlin, D-10117 Berlin, Germany; Berlin Institute of Health, D-10178 Berlin, Germany; Cluster of spikelets to assess their potential computational role in a Excellence NeuroCure, D-10117 Berlin, Germany; German Center for given system. Neurodegenerative Diseases (DZNE) Berlin, D-10117 Berlin, Germany; One factor that complicates (comparative) spikelet and Max-Delbrück-Centrum für Molekulare Medizin, Berlin, Germany studies and contributes to the confusion about their origin is Susanne Schreiber: Institute for Theoretical Biology, Department the many different names for spikelets that can be found in of Biology, Humboldt-Universität zu Berlin, D-10115 Berlin, Germany; Bernstein Center for Computational Neuroscience Berlin, the literature. These alternative names, sometimes reflect- Philippstr. 13, D-10115 Berlin, Germany; and Einstein Center for ing the presumed origin of spikelets, include the following: Neurosciences Berlin, D-10117 Berlin, Germany ‘IS spikes’ (IS: initial segment; Coombs et al., 1957), ‘fast Open Access. © 2019 Richard Kempter et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 Public License. 102 M. Michalikova et al.: Spikelets in pyramidal neurons Dendritic spikeGAxonal AP ap-junction couplingEphaptic coupling Figure 1: Mechanisms of spikelet generation. Somatic spikelets (blue traces) can result from propagation failures of dendritic spikes or axonal APs as well as from AP transmission through gap junctions or ephaptic transmission through extracellular fields. prepotentials’ (FPPs; Spencer and Kandel, 1961), ‘short- first spikelet type (Figure 2A, B) is characterized by rela- latency depolarizations’ (Llinas et al., 1974), ‘d-spikes’ (d: tively large amplitudes (typically in the range of 10 mV) dendritic; Wong and Stewart, 1992), ‘partial spikes’ (Zhang and fast rise dynamics (max. dV/dt of 10–40 V/s). The et al., 1998), ‘small spikes’ (Connors and Kriegstein, 1986), decay is often, but not always, biphasic, with an initial ‘third potentials’ (Kaplan and Shapley, 1984), and ‘ePSPs’ faster phase (time constant <1 ms) followed by a slower (electrical PSPs; Gibson et al., 2005). phase (time constant >5 ms; Figure 2A, B right). These The question of spikelet origin is resolved for some large-amplitude spikelets show an all-or-none behav- systems. For example, spikelets in cortical interneurons ior, and in a single cell there is usually one, rarely two, were found to result from electrotonic coupling by den- discrete amplitudes of spikelets (Schmitz et al., 2001; drodendritic and somatodendritic gap junctions, which Crochet et al., 2004; Epsztein et al., 2010; Chorev and increases the firing synchrony of interneurons and pro- Brecht, 2012; Coletta et al., 2018). The generation of these motes generation and maintenance of network oscilla- spikelets is voltage-dependent, where somatic hyperpo- tions (Bennett and Zukin, 2004). In contrast, the origin of larization suppresses the spikelets and somatic depolari- spikelets in cortical pyramidal neurons is still not settled. zation promotes the spikelet incidence (Crochet et al., Virtually all possible spikelet mechanisms have been 2004; Chorev and Brecht, 2012). Moreover, these large- hypothesized to explain spikelet occurrence in these cells, amplitude spikelets are sensitive to sodium channel but the experimental evidence is ambiguous. blockers, which suggests that they are actively propa- In this article, we focus on spikelets in cortical gating within the recorded cells (Schmitz et al., 2001; pyramidal neurons. We first describe the properties of Crochet et al., 2004). This spikelet type occurs as a single spikelets, noting that there are at least two qualitatively event or in bursts with short inter-spikelet intervals of distinct spikelet types occurring in these cells. Then, we few milliseconds (Figure 2B). Interestingly, the large- review the various mechanisms that can give rise to spike- amplitude spikelets can trigger somatic APs, which show lets. We present theoretical considerations about spikelet a distinct initial rising phase (‘shoulder’) that fits the properties generated by each of the possible mechanisms spikelet waveform (Epsztein et al., 2010). In CA1 pyrami- and compare them to experimental data from pyramidal dal neurons in vivo, firing rates of these spikelets show neurons. We also discuss the functional implications of spatial modulation with place fields virtually identical each type of spikelet. to the place fields of somatic APs (Epsztein et al., 2010). In presubicular head-direction cells, spikelets and APs from a single cell exhibit virtually identical head-direc- tion tuning (Coletta et al., 2018). Properties of spikelets in pyramidal A different type of spikelet was also found in both neurons neocortical (Figure 2C; Scholl et al., 2015) and hippocam- pal (Figure 2D; Valiante et al., 1995) pyramidal neurons. At least two qualitatively different spikelet types have These spikelets exhibit smaller amplitudes (typically been observed in cortical pyramidal cells (Figure 2). The in the range of 1 mV) and a brief time course (width at M. Michalikova et al.: Spikelets in pyramidal neurons 103 A Spikelets AP Spikelet EPSP EPSPs B 20 mV 3 mV APs 60 5 ms 100 ms AP 40 Spikelet 20 EPSP Spikelets Amplitude (mV) 0 0802160 40 –67 mV Maximum slope (dV/dt) C 3 4 3 Start 2 2 AP 2 End 1 1 0 0 0 –1 –2 –1 ential (mV) t Spikelet po 1 6 4 0.5 3 2 0 0 0 Membrane 0.5 –1 –3 –2 10 mV 50 ms 02.5 5 02.5 5 02.5 5 Time (ms) Time (ms) Time (ms) D Integrate Figure 2: Two types of spikelets observed in pyramidal neurons. (A, B) Large-amplitude spikelets recorded in vivo in putative pyramidal cells in cat neocortex (A; Crochet et al., 2004) and in hippocampal CA1 pyramidal neurons (B; Epsztein et al., 2010). Left: Example somatic voltage
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