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Cellular/Molecular

Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms

Abdallah Hayar, Michael T. Shipley and Matthew Ennis
Journal of Neuroscience 7 September 2005, 25 (36) 8197-8208; https://doi.org/10.1523/JNEUROSCI.2374-05.2005
Abdallah Hayar
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Michael T. Shipley
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Matthew Ennis
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  •   Figure 1.
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    Figure 1.

    TTX sensitivity of spontaneous EPSCs in ET cells. A, Voltage-clamp recordings (HP of –60 mV) of an ET cell, showing the effect of TTX (1 μm) on spontaneous EPSCs. The inset at right shows a Neurolucida drawing of the ET cell. Note the highly branched tufted dendrites that ramify throughout a large portion of a single glomerulus (closed line). The thin lines above and below the cell indicate boundaries of the glomerular layer with the olfactory nerve layer and external plexiform layer, respectively. B, Scatter plot of the amplitude of EPSCs of the ET cell shown in A. TTX preferentially eliminated relatively large amplitude EPSCs. C, D, Histograms of inter-EPSC time interval and amplitude distributions, respectively, for the ET cell shown in A. Also shown are the cumulative probability distributions, which indicate significant difference between control and TTX (p < 0.0001, K–S test). The largest 10% of the EPSCs (dashed horizontal line in D) were eliminated by TTX.

  •   Figure 2.
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    Figure 2.

    Spontaneous bursts of IPSCs in ET cells. A, Voltage-clamp recordings from an ET cell (HP of 0 mV) show that spontaneous IPSCs occur mostly in bursts. APV (50 μm) reduced the IPSC burst frequency; subsequent application of CNQX (10 μm) eliminated the bursts. Additional application of gabazine (10 μm) blocked all of the remaining IPSCs. B, Group data (n = 8) showing the effect of the blockers on the frequency of IPSCs, the IPSC burst frequency, and the number of IPSCs per burst. Data obtained during drug application were compared with those obtained before drug application using paired t test (*p < 0.01; **p < 0.001). C, Autocorrelograms of IPSC trains obtained from 5–6 min recordings from six ET cells. Thicker black trace and the gray curve represent the average autocorrelogram and the single decay exponential fit, respectively. The decay time constant, 40 ms, estimates the duration of the average IPSC burst. D, Autocorrelogram of IPSC trains from one ET cell obtained in control, during application of APV, and after additional application of CNQX. Note that the autocorrelogram in APV and CNQX becomes noisy because of a reduction in the frequency of IPSCs and did not show a significant peak.

  •   Figure 3.
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    Figure 3.

    Pattern of spontaneous and evoked EPSCs and IPSCs. A–D, F, and G were obtained from the same cell. A, An ET cell was first recorded extracellularly, and then (in B) the same cell was recorded intracellularly in voltage clamp (HP of –30 mV) using a patch pipette containing CsMeSO3 and QX-314. The cell displayed relatively large amplitude EPSCs (downward deflections), followed by bursts of IPSCs (upward deflections). C, Superimposed traces (n = 20) were triggered on relatively large spontaneous EPSCs. Most of the EPSCs were followed by a cluster of IPSCs (dark gray line is a typical example). The average (light gray line) of 150 such traces indicates that a significant outward current followed the EPSCs. D, Scatter plot of the peak amplitude of IPSCs versus the amplitude of the preceding EPSC. The linear curve fit (gray line) indicates significant positive correlation. E, Averaged trace (thicker line) of the mean of 100–200 EPSC–IPSC traces as obtained in C from five ET cells. The average trace indicates that the outward current of the IPSCs peaked at 63 ms from the onset of the EPSC and decayed with a time constant of 68 ms. F, Olfactory nerve layer stimulation evoked the same sequence of currents; short-latency EPSC, followed by a burst of IPSCs. At the holding potential of 0 mV (near the reversal potential of excitatory ionotropic receptors), only the IPSCs were observed. G, Photograph of the ET cell filled with the Lucifer yellow during recording (note stimulation electrode at top left). H, ON stimulation (55 μA) evoked a fast EPSCs followed by a slow EPSCs, whereas EPL (550 μA) stimulation evoked only slow EPSCs. All evoked EPSCs were reversibly blocked by APV and CNQX. Five superimposed traces are shown in each stimulation condition. Stimulation artifacts were truncated for clarity.

  •   Figure 4.
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    Figure 4.

    Synchronous slow and fast EPSCs in ET cells of the same glomerulus. All data presented in this figure were obtained from the same ET cell pair. A, Simultaneous extracellular recordings from two ET cells with correlated spike bursting (correlated spikes shown in the inset at right). B, The same two cells were then recorded in whole-cell configuration in voltage clamp (HP of –60 mV) using electrodes (containing CsMeSO3 and QX-314). Note the synchronous slow (horizontal lines with arrows on both sides) and fast (asterisks, example shown at right) EPSCs. C, Cross-correlogram of the spike trains (5 min recording sample, 1 ms bins) shows a significant correlation with a peak near zero lag time (see inset). D, The cross-correlogram of the membrane current (50 s of intracellular recording sample, 2 ms bins) shows both a broad (small lines with arrows on both sides) and narrow (asterisk, see inset) correlation that peaked at zero time lag. The gray trace is the cross-correlogram of the membrane current traces after shifting the second trace by 5 s (to determine significance, see Materials and Methods). E, Cross-correlogram of the EPSC trains (5 min recording sample, 1 ms bins) shows a significant peak only in the bin at zero time lag, indicating synchronous EPSCs in the two recorded cells. F, Cumulative probability histograms of the EPSC amplitudes of synchronous and asynchronous EPSCs recorded in both cells (during 5 min). The synchronous EPSCs exhibited significantly larger amplitude than asynchronous EPSCs (p < 0.0001, K–S test). G, Scatter plot of the amplitude of synchronous EPSCs in cell 2 versus cell 1 and a linear regression fit showing a significant positive correlation. H, Photograph of the two recorded cells after biocytin staining showing the overlap of dendrites in the same glomerulus (dashed line).

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    Figure 5.

    Synchronization in burst firing is attributable in part to a synchronous, action potential-dependent excitatory input. A, B, Simultaneous recordings from two pairs of ET cells whose dendrites ramify in the same glomerulus. Red and blue traces correspond to recordings of the two cells, respectively; the blue cell was subsequently recorded in voltage-clamp mode (bottom 2 panels). A1, The two cells exhibited synchronous spike bursts at resting potential; asterisks here and in the panels below indicate synchronous events. A2, When both cells were hyperpolarized using current injection, they displayed synchronous EPSPs. A3, The synchronous EPSP/Cs were relatively large and disappeared in TTX (A4); reconstruction at right shows that the two ET cells were associated with the same glomerulus. B, Traces obtained from two other simultaneously recorded ET cells (first cell, current-clamp recording in red; second ET cell, voltage-clamp recordings at an HP of –60 in blue); a 40 pA EPSC threshold was used for triggering because larger EPSCs are more likely to be driven by action potentials in presynaptic terminals. The scatter plot from such recordings shows that EPSCs smaller than 80 pA in the ET cell (blue) were rarely associated with a corresponding EPSP in the other ET cell (red; i.e., the amplitude of EPSPs is near 0 mV). In contrast, when the EPSC amplitude exceeded 80 pA, there was typically a large synchronous EPSP in the red cell (inset). Reconstruction at right shows that the two ET cells were associated with the same glomerulus.

  •   Figure 6.
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    Figure 6.

    Synchronous bursts of IPSCs in ET cell pairs. All data in this figure were obtained from the same ET cell pair. A, Simultaneous whole-cell voltage-clamp recordings (HP of 0 mV) from two ET cells (gray and black traces, respectively) show synchronous IPSC bursts (asterisks) before and during application of APV (50 μm). Note that, although APV reduced burst frequency, bursts remained synchronous in the two cells. Additional application of CNQX eliminated the IPSC burst synchrony. Areas highlighted in rectangles are shown at faster timescale at right. B, Membrane current cross-correlograms (50 s recording samples, 2 ms bins) in control, APV, and after additional application of CNQX. The cross-correlograms of currents indicate the degree to which changes in membrane current of each cell were correlated (see Materials and Methods). Note the significant peak (confidence limit >99.73%) at zero lag time in control and APV. There was no significant correlation after application of CNQX. The 99.73% confidence limit was determined by cross-correlating traces shifted by 5 s (dashed traces; see Materials and Methods). C, Cross-correlogram of the IPSC trains (5 min recording samples, 1 ms bins) show a significant narrow peak (see in set) at zero time lag, indicating synchronous IPSCs in the two recorded cells. The cross-correlograms of IPSCs indicate how frequently one cell exhibits synchronous IPSCs with another cell compared with chance (see Materials and Methods). The narrow peak was superimposed on a broader peak corresponding to the longer duration correlated IPSC bursts. CNQX abolished correlation and synchrony of IPSCs. D, Simultaneous whole-cell voltage-clamp recordings (HP of –30 mV) from the same two ET cells showing synchronous EPSCs followed by IPSC bursts; recording highlighted in rectangle is shown at faster timescale at right. Recordings obtained before the application of synaptic blockers in A. E, Membrane current cross-correlogram (50 s sample, bin of 2 ms) at an HP of –30 mV shows the significant biphasic cross-correlation (positive peak C = 0.19 at 0 lag time; negative peak C = 0.10 at 72 ms lag time); dashed trace represents the cross-correlogram of the two currents after shifting the traces by 5 s. F, Photograph showing Lucifer yellow labeling of the two recorded cells.

  •   Figure 7.
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    Figure 7.

    Activity of ET cells affiliated with adjacent glomeruli is not correlated. All data presented in this figure were obtained from the same ET cell pair. A, Simultaneous extracellular recordings were obtained from two ET cells, and then the same two cells were recorded in whole-cell configuration (B) in voltage clamp (HP of –60 mV) using electrodes containing CsMeSO3 and QX-314. Note the absence of synchronous EPSCs. C, Recordings from the same cells at an HP of 0 mV show no synchronous IPSCs. D, Cross-correlograms of the spike trains (5 min sample, bin of 1 ms) show that action potentials were not correlated. E, F, Membrane current cross-correlograms (50 s samples, 2 ms bins) show that there was no correlation of EPSCs (E; HP of –60 mV) or IPSCs (F; HP of 0 mV). The gray dashed traces indicate membrane current traces after shifting traces by 5 s (to determine significance, see Materials and Methods). G, Biocytin staining indicated that the dendrites of the two ET cells were affiliated with different glomeruli (dashed lines).

  •   Figure 8.
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    Figure 8.

    ET cells communicate via gap junctions. A–D were obtained from the same ET cell pair. A, Simultaneous extracellular recordings from two ET cells with apparent correlated bursting. B, Cross-correlogram of the spike trains (5 min, 1 ms bins) shows significant broad synchrony at approximately zero time lag. C, Both cells were recorded simultaneously in whole-cell voltage-clamp mode at an HP of –60 mV using pipettes containing CsMeSO3 and QX-314. Each cell was stimulated with a positive voltage step (100 ms from –60 to –20 mV) to generate a calcium current. The calcium currents triggered a slow inward current in the other cell and a post-pulse inward current in the same cell. The occasional failures (arrows) and response variability contrasts with the putative gap junction currents shown in D. D, The existence of gap junction currents was tested between the two ET cells by generating 50 mV negative voltage step pulses (200 ms from –60 to –110 mV) in each cell and measuring the current evoked in the other cell. This produced an outward current in the other cell (asterisks); note that the current exponentially reached a steady-state level of ∼10 pA. C and D show six representative current traces from each cell in each condition and an average of 20 traces (thick gray line). Areas highlighted in rectangles are expanded in the insets shown at bottom. E, F, Recording in an ET cell of responses to application of positive and negative voltage steps in another ET cell affiliated with the same glomerulus. E, CNQX and APV blocked the synaptic currents (noisy signal in control) and revealed an underlying inward current that extended beyond the stimulation pulse. The evoked current was inhibited by carbenoxolone (300 μm), and this effect was only partially reversible, as shown in inset at top right (the line represents a running average of the electric charge of 30 evoked currents). F, The negative voltage steps produced an outward current and a rebound oscillation that were inhibited by carbenoxolone. Each trace is an average of 50 traces in each condition.

  •   Figure 9.
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    Figure 9.

    ET cells of the same glomerulus exhibit synchronous, spontaneous gap junction currents. A, Simultaneous extracellular recordings from two ET cells showing spontaneous bursting discharge before and during application of fast synaptic blockers and then after additional application of the calcium channel blockers cadmium and nickel. Spike train cross-correlograms (5 min sample in each condition) at right show that burst synchrony persisted in the presence of blockers of fast synaptic transmission and calcium channels. B, Current-clamp recordings from an ET cell in the presence of synaptic blockers using a pipette that contains QX-314 (10 mm). Note spontaneous membrane potential oscillations and small spikelets. Hyperpolarization (bottom trace) did not affect the frequency of the oscillations or the spikelets. Recording samples indicated by rectangles are shown at faster timescale at right in this and bottom panels. C, Recordings from another ET cell in voltage clamp (HP of –60 mV, using pipette containing CsMeSO3 and QX-314) show that the spikelets and the membrane current oscillations persisted in the presence of the calcium channel blockers. D, Simultaneous recordings from an ET cell pair recorded in the presence of synaptic blockers. Note the synchrony between the membrane current oscillations as well as between the spikelets. The gap junction blocker carbenoxolone progressively decreased the frequency and amplitude of the synchronous oscillations and spikelets before a complete blockade occurred after 7 min. Bottom right panel shows the membrane current cross-correlogram (50 s samples, 2 ms bins) in control and during application of carbenoxolone.

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    • supplemental material - Figure S1. Schematic model of ET-ET and ET-PG-ET cell interactions. ET cells (right) exhibit synchronous spike bursting activity because they are connected by gap junctions (oval). ET cells (left) are synchronized further by synchronous EPSPs from the same olfactory nerve (ON) axons, and by correlated bursts of IPSPs from the same and different sets of periglomerular (PG) cells. The EPSPs and IPSPs occur in sequence and they respectively trigger and subsequently terminate the bursting. Mitral and tufted (M/T) cells may also be synchronized by similar interactions with ET and PG cells (question marks). Short axon (SA) cells have dendrites and axons extending throughout several glomeruli and thus might serve for inter-glomerular inhibition.
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The Journal of Neuroscience: 25 (36)
Journal of Neuroscience
Vol. 25, Issue 36
7 Sep 2005
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Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms
Abdallah Hayar, Michael T. Shipley, Matthew Ennis
Journal of Neuroscience 7 September 2005, 25 (36) 8197-8208; DOI: 10.1523/JNEUROSCI.2374-05.2005

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Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms
Abdallah Hayar, Michael T. Shipley, Matthew Ennis
Journal of Neuroscience 7 September 2005, 25 (36) 8197-8208; DOI: 10.1523/JNEUROSCI.2374-05.2005
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