EXPERIMENTALNEUROLOGY

108,76-82

(1990)

In Viva Electrophysiological Analysis of Lucifer Yellow-Coupled Hippocampal Pyramids ANGEL NiTtiz,* *Departamento

de Inoestigaci&,

Hospital

ELIO GARCIA-AUSTT,* “Ram&y

Cajal”and

tLaboratorio

INTRODUCTION

Although controversy exists (e.g., (9, 17)), independent lines of evidence indicate electrotonic coupling in CAl, CA3 pyramidal neurons and dentate granule cells. The dye lucifer yellow (LY) crosses gap junctions in many systems (3, 4, 6, 32, 34, 35). LY dye-coupling has been demonstrated in vitro and in vivo in CAl, CA3 pyramidal cells and in vitro in dentate granule neurons (2, 19, 21, 22). Gap junctions have been shown on apical dendrites and somata of rat CA3 pyramidal neurons (28) and dentate granule cells (21). Electrotonic coupling was shown in vitro in simultaneously impaled pyramidal cells and in granule cells (20, 21, 26). Small, transient all-or-none depolarizations, also termed spikelets,

0014-4886/90

Inc. reserved.

Znstituto

Cajal,

CSIC,

Madrid,

Spain

The preparation has been described previously (25). Briefly, EEG recordings were made in the dorsal hippocampus (A 3.5, L 3.0, H 2.5) in 55 urethane anesthetized (1.5 g/kg ip) and curarized (l-2 mg/kg ip) SpragueDawley rats, weighing 200-300 g. Electric stimulation was in the dorsal fornix (A 5.7, L 1.5, H 3.0) and perforant path (A 0.0, L 4.5, H 2.5). Micropipets filled with 5% LY in 1 M LiCl(150-250 MQ) were used for intracellular staining and recording. Three molar K-acetate filled 76

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de Neurofisiologia,

BuRof-’

METHODS

should be addressed at Neurofisiologia, Arce 37, E-28002, Madrid, Spain.

Copyright 0 1990 by Academic Press, All rights of reproduction in any form

WASHINGTON

pseudospikes, d-spikes, or short latency depolarizations (e.g., (14, 18, 29, 31, 37)), were a common finding in the hippocampus where they usually preceded spikes and were termed fast prepotentials (20, 21, 33). They have been attributed in simultaneously impaled pyramidal neurons and in granule cells to spikes electrotonically propagated through gap junctions (20,21). Bulloch and Kater (6) have shown that lesioned axons in Helisoma form new electrotonic junctions, and Gutnick et al. have shown (13) that in neocortical “slices” dye-coupling may depend on the plane of section. Therefore, dye-coupling may be an artifact of the slice technique due to lesioned axons and/or dendrites and subsequent cell fusion. Dye-coupling has been shown by MacVicar et al. (22) in vivo in the hippocampus; therefore this type of artifact is unlikely. However, the lack of electrophysiological correlates in their 10 dye-injected cells and the selection criteria they used (Ref. (22)), which rejected cells with membrane potential < 30 mV, does not completely eliminate the possibility that some of their five coupled casesmay also have been injured. To our knowledge there is no in vivo demonstration of correlation between dye-coupling and spikelets in hippocampal pyramidal cells. Such a correlation would provide strong indirect evidence in favor of electrotonic coupling. The possible participation of coupling potentials in theta-rhythm genesis, suggested by others (e.g., (20, 21)), should also be tested. We therefore analyzed the association between spikelets and LY dye-coupling and the relation of spikelets with theta. A preliminary version of this work has been published in abstract form (24).

Small transient all-or-none depolarizations (also termed in the literature fast prepotentials, spikelets, pseudospikes, d-spikes, or short latency depolarizations) and their association with lucifer yellow (LY) dye-coupling were analyzed in CAl-CA3 hippocampal pyramidal cells in urethane anesthetized rats. It was found that (a) 15 of the 24 LY-injected pyramidal neurons (63%) showed dye-coupling; (b) spontaneous, antiand orthodromically evoked spikelets (3-7 ms in duration; 3- to 12-mV peak) were recorded in 40 of 95 cells (42%); (c) there was a significantly higher probability of dye-coupled neurons with spikelets and of uncoupled ones without spikelets; (d) spikelet waveform and amplitude were unaffected by spontaneous or imposed polarizations; (e) large hyperpolarizations could reduce the rate and even prevent spikelets; and (f) spikelets could precede or follow spikes, the latter were more frequent with large depolarizations. Electrophysiological findings, and the association of dye-coupling and spikelets, suggest strongly that at least some spikelets are coupling potentials. This implies that pyramidal cells may be electrotonically coupled under physiological conditions. 0 1990 Academic Press, Inc.

1 To whom correspondence Instituto Cajal, Av. Doctor

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IN VIVO DYE-COUPLING

capillaries (50-90 MQ) were also used. LY was injected ionophoretically using 0.5- to l.O-nA, 500-ms, inward current pulses, repeated at 1 Hz for about 10 min. By at least 20 min after LY injection animals were deeply anesthetized and the brains were perfused transcardially with saline and fixed in 10% formaldehyde in 0.1 M phosphate buffer for 24 h. Sections (75 pm) mounted in Entellan (Merck) were photographed in a fluorescence microscope. Data were stored on FM tape for subsequent analysis. Spikelet- and spike-triggered hippocampal EEG averages were calculated off-line in a digital computer to estimate temporal correlations. RESULTS

Electrophysiological characteristics and cell selection criteria. The neurons selected (37 CA1 and 58 CA3 cells) were held under stable conditions for at least 20 min. They showed resting membrane potentials more negative than -50 mV (mean, 59.5 mV; SD, 7.6), spikes of 40 mV or more (mean, 63.7 mV; SD, 10.5), and input resistances of 28.3 MO (SD, 8.5) and 37.5 MO (SD, 9.7) for CA1 and CA3 neurons, respectively. Eighty-three percent of the cells fired overshooting spikes. All cells discharged spikes spontaneously (mean rate, 11 spikes/ s; SD, 7.3). These values suggest intrasomatic recordings (2, 17, 33) and are similar to those of other in uiuo (e.g., (16,22,25)) and in vitro (Refs. (2, 17,29,39)) pyramidal neuron recordings. Therefore, cells meeting these criteria were considered healthy; all others were eliminated from the sample. Twenty-four cells were stained with LY and identified as pyramidal cells, on the basis of their morphology, situation of the soma in the stratum pyramidale, and apical and basilar dendrites in the stratum radiatum and oriens, respectively. We were unable to dye-fill nonpyramidal cells. Eighty-one of 95 cells (or 85%) were driven antidromically; 17 were also identified by intracellular LY injection. Nonpyramidal projection cells are very scarce (1); therefore, unstained antidromically driven neurons were also probably pyramidal neurons. “Unidentified” cells (n = 14) that could not be driven antidromically and were not stained intracellularly, but had similar electrophysiological characteristics, were probably pyramidal cells. Forty of the 95 neurons (or 42%) also displayed spikelets described in detail below. The population of dyecoupled cells without spikelets and the population of neurons with spikelets had resting potentials of -58.6 mV (SD, 2.4) and -61.9 mV (SD, 10.4), action potential amplitudes of 55.0 mV (SD, 14.1) and 65.3 mV (SD, 8.7), and input resistances of 30.9 MQ (SD, 8.2) and 35.3 MQ (SD, 5.8), respectively. They could not be differentiated electrophysiologically from the rest of the neurons. This also implies that injected pyramidal neurons were unaffected by LY and lithium.

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Dye-coupling. LY injections revealed 7 of 12 CA1 (or 58%) and 8 of 12 CA3 (or 67%) dye-coupled pyramidal neuron aggregates (62% of all injected cells). They either had 2 (n = 10, or 67%) or 3 (n = 5, or 33%) pyramidal cells with well-spaced somas and extensive overlapping dendritic arborizations (Figs. 1A and 1B); proportions were similar for CA1 and CA3 subfields. Dye-coupled CA3 pyramidal neurons sometimes appeared in tight bundles (e.g., Fig. lC), which were never seen in the CA1 region. Some injected neurons were intensely stained but did not dye-couple, as the CA1 pyramidal cell shown in Fig. 1D (cf. (25)). Examples of recordings from dyecoupled cells are shown in Figs. 2,3, and 5D. We did not observe dye-coupling with nonpyramidal neurons. Spikelets. The spikelets recorded in 40 (11 CA1 and 29 CA3) pyramidal cells, or 42% of all recorded cells, were usually transient (3-7 ms), 3- to 12-mV (mean, 10.2 mV; SD, 6.2) all-or-none depolarizing events (Fig. 2A), with brief rising (mean duration, 0.87 ms; SD, 0.11) and falling (mean duration, 4.17 ms; SD, 3.81) slopes (e.g., Refs. (20, 33)). Some cells showed qualitatively similar but smaller events < 3 mV (cf. 37)) which were not considered spikelets because they were within the noise level which was large as in other in uiuo pyramidal cell recordings (25). Although in a given pyramidal neuron spikelet amplitude varied slightly (1.5 nA)

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1. Lucifer yellow-injected pyramidal cells. (A, B) Dye-coul )led CA1 cells. (C) CA3 pyramidal (B) Reconstruction; two successive sections. Horizontal calibl ration bars, 50 pm.

could Ireduce spikelet rates or even abolish spikelets shown ; cf. (11)). Spikelet amplitude and waveform unaffe’ cted by imposed transmembrane currents.

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Spikelets could occur in bursts at very sho ‘z-t delays (~2 ms). In some cases, and more frequently in tE te CA3 subfield, spikelet bursts “rode” on slow depola rriz :ations

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IN VZVO DYE-COUPLING

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Stained Neurons and Spikelets in Hippocampal Pyramidal Cells With Coupled Uncoupled Total

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FIG. 2. Spontaneous conditions. (A) Spikelets occurred at all potential values and triggered spikes above a threshold (upper). (B) Above threshold (lower) a spikelet triggered a spike (prepotential); when depolarized (upper) the firing sequence was inverted (postpotential). Records from the coupled CA3 pyramidal cell shown in Fig. 1C.

(Figs. 4A and 4B; cf. (25,30,39)). Spikes were triggered when spikelets in the burst reached a threshold potential (arrows in Fig. 4B; cf. (29)). Fornix and perforant path stimulations evoked the well known EPSP-IPSP sequence (Fig. 5D; cf. (16)). In a few cells (n = 6 or 5%), as in Fig. 5A with fornix stimulation, antidromic spikes (arrow 1) were elicited (17,37). Antidromic spikelets reappeared (arrow 2) when the antidromic spike was blocked by a previous spontaneous spike (i.e., collided). In Fig. 5B, spikelets were elicited at a lower threshold than the antidromic spike. Under

spikelets

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9 9

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6

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24

those conditions, low stimulus intensities evoked EPSPs (arrow 1). Above a threshold intensity spikelets were elicited at very brief latencies (arrow 2). With higher intensities antidromic spikes were triggered (arrow 3). In other cells, as shown in Fig. 5C with perforant path stimulation, spikes or spikelets were orthodromically evoked at the peak of the EPSP. Orthodromic spikelets had waveforms and amplitudes similar to those of spontaneous and antidromic ones (cf. (9)). Spikelets were always absent during stimulus evoked IPSPs (i.e., “recurrent IPSPs), as with fornix stimulation in Fig. 5D, but reappeared during the subsequent depolarization. However, spikelets could be present during spontaneous or imposed hyperpolarizations of magnitudes as those of IPSPs (cf. Figs. 1 and 2). During theta, CA1 and CA3 pyramidal cells usually displayed smooth potential oscillations at theta frequency (Fig. 6A; cf. (25)). Spikes and spikelets (arrows) occurred only during the depolarizing intracellular-theta wave. This behavior is clearly different from the spontaneous condition when spikelets could also occur at more hyperpolarized values. EEG averages revealed that spikelets (B) and spikes (C) tended to occur in close temporal correlation with theta. Spikelets usually triggered spikes under those conditions.

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FIG. 3. Effects of imposed current. Control (middle), spikelets occurred at all potentials and triggered spikes above a threshold (arrows); depolarizing current (upper) decreased spikelet-spike delays (first arrow) and could generate postpotentials (second arrow); hyperpolarizing current blocked spikes but not spikelets (lower). CA1 coupled cell. Horizontal arrows indicate the “resting” potential.

FIG. 4. Spontaneous spikelet bursts. (A) Spikelet bursts “riding” on a slow depolarization triggered spikes (arrows). (B) Spikelet bursts on smaller depolarizations triggered spikes (arrows). Note similarities between superimposed records in B. CA3 neurons.

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FIG. 5. Stimulus elicited spikelets. (A) Fornix stimulation, antidromic spike (l), when blocked unmasks an antidromic spikelet (2). (B) Low intensity evoked an EPSP (l), intermediate intensity an antidromic spikelet (2), and higher intensity a spike (3), CA1 neuron. (C) Perforant path stimulation; high intensity evoked an EPSP and a spike (1); at lower intensity the EPSP was “topped” by a spikelet (2). (D) Fornix stimulation, antidromic spike and EPSP-IPSP followed by spikelets (arrows) and spikes. (C, D) Coupled CA3 cells. Vertical arrows, stimuli.

DISCUSSION

Our most relevant findings were the in uivo demonstration of a statistically significant association between dye-coupling and spikelets and the indirect electrophysiological evidence indicating that at least some spikelets are coupling potentials. This implies that pyramidal cells may be electrotonically coupled under physiological conditions. The results also provide support for a synchronizing role of coupling during theta. Although we cannot completely reject artifactual LY dye-coupling in our sample, it appears very unlikely since (a) the morphology of coupled pyramidal neurons was normal and they were not disrupted; (b) nonpyramida1 cells and glial cells would also uptake the leaked LY, but only pyramidal neurons were stained; (c) clear-cut separations between somas of an aggregate were usual, and since the soma is the most likely place of impalement, leakage into neighboring pyramidal cells is unlikely; (d) electrophysiological criteria indicate healthy neurons (see Results). In agreement with other reports (2,19,22), about 50% of the injected pyramidal neurons did not dye-couple, because they did not have gap junctions, coupling ratios were low (23), or cells of that aggregate had uncoupled (cf. (27)). The spikelets described above were similar to those observed in other CNS regions (e.g., (14, 31, 36)). They have usually been interpreted as active all-or-none events generated far from the recording site, in either the impaled or the coupled neurons (9, 17, 20, 21, 33). Some dye-coupled cells did not show spikelets, either be-

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cause they were small (~3 mV; see Results), occurred during spike peaks and remained undetected, and were silent, or because gap junctions rectified (10). Electrophysiologically, the principal support in favor of the coupling nature of spikelets was that they could be elicited antidromically (Figs. 5A and 5B), representing antidromic spikes generated in neighboring cells and conducted electrotonically through gap junctions (2, 11, 12,37). In the work of Spencer and Kandel(33), the lack of antidromic spikelets was the main evidence that spikelets reflected dendritic spikes. Antidromic spikelets, however, were only seen if the coupled pyramidal cell fired when the impaled cell was silent (see also (21)). This occurred with a lower spike threshold in the coupled than in the impaled neuron or when antidromic spikes were blocked by a previous spontaneous spike (i.e., collided). Antidromic and spontaneous spikelets were identical; therefore, the former were not the intracellular reflection of the extracellular “population spike” (15, 38). Further evidence comes from the slice preparation where antidromic spikelets could be evoked after blocking chemical transmission, indicating that they are not transient EPSPs nor synaptically evoked distant spikes in the impaled cell (Refs. (2,12)). Spikelets could occur during the repolarizing phase of a spike (Figs. 2B and 3; cf. (21,29,33,37)). Thus, spikelets were unaffected by the refractory period of the impaled cell, indicating that they did not reflect distant spikes or axon-hillock spikes in the impaled pyramidal cell. Although very unlikely, spikelets may have origi-

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FIG. 6. Spikelets during theta. (A) EEG and intracellular records (upper and lower, respectively); spikes and spikelets (arrows) only on the positive intracellular and negative EEG waves. (B) Spikelet-triggered EEG averages. (C) Spike-triggered EEG averages. Vertical arrow and lines in B and C indicate the trigger references. CA3 pyramidal cell.

IN VZVO DYE-COUPLING

nated in the impaled cell (17) as an “M-spike” (5), an antidromic spike in an axon collateral not invaded by the soma spike. In coupled cell aggregates without rectifying synapses one would expect that under spontaneous conditions when excitability is similar in all coupled neurons the impaled pyramidal neuron would fire before or after coupled pyramidal cells with equal probability. In that state it is equally likely that a coupled spike triggers an impaled cell spike or the opposite sequence. In our sample large depolarizations increased the probability of postpotentials. This implies that spikes in the depolarized cell (not preceded by spikelets) triggered spikes in the coupled neuron which were reflected as postpotentials in the impaled pyramidal neuron. The sequence would consist of a spike followed by a postpotential in the depolarized impaled cell and a spikelet followed by a spike in the coupled pyramidal cell (see Fig. 6B in Ref. (21)). Strong hyperpolarizing currents could reduce the rate and even abolish spikelets, probably because they hyperpolarized coupled cells below firing threshold (11, 20, 21). Therefore, their origin is probably not the impaled cell. This does not necessarily rule out that some spikelets may be remote dendritic Na+ spikes originating in the impaled neuron, which due to the space constant may be unaffected by the injected current (9, 17, 33). However, spikelets were absent during recurrent IPSPs (Fig. 5D), probably because they were abolished only when all pyramidal cells of an aggregate were silenced by the IPSP. Spikelets usually persisted with spontaneous or imposed hyperpolarizations of similar magnitudes that did not silence all the aggregate. This implies that spikelets are coupling potentials. Spikes and spikelets occurred at the depolarizing intracellular-theta wave (Fig. 6), probably reflecting that they were spikes triggered in coupled cells by synchronous EPSPs (e.g., (25)). The close temporal correlation between rhythmic spikes and spikelets is not surprising given the usual firing synchrony of pyramidal neurons during theta (7, 8). Electrotonic interactions through gap junctions evoked by spikelets and also probably by slower potentials may contribute to synchronous firing in pyramidal cell aggregates during theta. ACKNOWLEDGMENTS A.N. is the recipient of a FISS (Ministerio de Sanidad y Consumo) fellowship. This work was partly supported by FISS Grant 86/599 to E.G.-A., and a DGICYT grant to W.B.

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In vivo electrophysiological analysis of lucifer yellow-coupled hippocampal pyramids.

Small transient all-or-none depolarizations (also termed in the literature fast prepotentials, spikelets, pseudospikes, d-spikes, or short latency dep...
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