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1 Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo 113-0033, Japan
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Abstract |
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5 Hz) and gamma (40 Hz). Such field oscillations, however, are not merely a result of coherent neuronal activity. They may also play active roles in information processing in the brain. In this study, we observed that, in cultured hippocampal slices, CA3 pyramidal cells responded to single-pulse stimuli with monosynaptic and polysynaptic potentials and firing spikes which occurred after variable latencies. The variability of the spike latencies was greatly reduced in the presence of weak electric field oscillations, especially the oscillation in the gamma-band frequency range, that per se induced only small fluctuations in the subthreshold membrane potential, and this effect was inhibited by blockade of NMDA receptor activity. Furthermore, the latency of the firing spikes changed if the stimulus was applied at a different phase of the imposed gamma oscillations. These results may suggest that the background field oscillations serve as an extracellular time reference and assure accurate and stable decoding of a memory trace present in cortical feedback networks.
(Received 15 April 2004;
accepted after revision 9 September 2004;
first published online 16 September 2004)
Corresponding author Y. Ikegaya: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: ikegaya{at}tk.air.jp
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Introduction |
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Previous studies have mainly focused on the mechanisms underlying the induction and maintenance of the persistent activities, and little is known about readout from these activities. Buonomano (2003) has recently shown that in cultured neocortical slices, a memory trace present in the cortical circuit can be retrieved as a late suprathreshold response even after tens or hundreds of milliseconds. In his study, however, spike output timing was extensively jittered from trial to trial (standard deviation (S.D.) was up to 100 ms), indicating that the cortex seems unable to process information with temporal precision. The biophysical law of synaptic plasticity requires millisecond precision (Markram et al. 1997; Bi & Poo, 1998). We thus think that there might be a certain cellular mechanism that enhances temporal fidelity of the readout process to a point that meets the requirement of the physiological constraints.
One of the characteristic behaviours of hippocampal neurones is synchronous population activity (Harris et al. 2003), which causes periodic oscillations in extracellular electric fields. According to frequency, the oscillatory activity is categorized into distinct states, e.g., theta (5 Hz) and gamma (40 Hz). Artificially applied weak electric fields have been shown to be capable of modulating cortical activity both in vivo and in vitro (for review, see Jefferys, 1995), so we hypothesize that these electroencephalographic oscillations may enhance spike precision. By recording intracellular responses of CA3 pyramidal cells in hippocampal slice cultures, we examined the effect of field oscillations on the readout process. The results may be relevant to the possible mechanisms of persistent activity during short-term memory and shed light on the mechanisms by which network activity influences neuronal processing.
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Methods |
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Hippocampal slices prepared from postnatal day 7 Wistar/ST rats (SLC, Shizuoka, Japan) were cultured as previously described (Ikegaya, 1999). Briefly, rat pups were chilled, and the brains were aseptically removed, according to the National Institutes of Health guidelines for laboratory animal care and safety. The caudal half of the whole brain was horizontally cut into 300-µm-thick slices using a DTK-1500 vibratome (Dosaka, Kyoto, Japan) in aerated, ice-cold Gey's balanced salt solution (Invitrogen, Garthersburg, MD, USA) supplemented with 25 mM glucose. The entorhino-hippocampi were dissected out under stereomicroscopic controls and cultivated using the membrane interface technique, in which they were placed on sterile 30-mm-diameter membranes (Millicell-CM, Millipore, Bedford, MA, USA). Cultures were fed with 1 ml of 50% minimal essential medium (Invitrogen, Gaithersburg, MD, USA), 25% horse serum (Cell Culture Laboratory, Cleveland, OH, USA) and 25% Hanks' balanced salt solution (Garthersburg) and were maintained in a humidified incubator at 37°C in 5% CO2. The medium was changed every 3.5 days. Electrophysiological experiments were performed at days 9–20 in vitro.
Electrophysiological recordings
Whole-cell recording was performed as described elsewhere (Fujisawa et al. 2004). A cultured slice was transferred to a recording chamber and continuously perfused with oxygenated artificial cerebrospinal fluid consisting of (mM): 124 NaCl, 25 NaHCO3, 3 KCl, 1.24 KH2PO4, 1.4 MgSO4, 2.2 CaCl2 and 10 glucose (25°C). Micropipettes (4–7 M
) were filled with internal solutions consisting of (mM): 136.5 KMeSO4, 17.5 KCl, 9 NaCl, 1 MgCl2, 10 HEPES, 4 MgATP, and 0.2 EGTA (pH 7.2). Tight-seal whole-cell recordings were obtained from CA3 pyramidal neurones under IR-DIC microscopy. Recordings were carried out with an Axopatch 200B amplifier (Axon Instruments, Union City, CA, USA). Signals were low-pass filtered at 1 kHz, digitalized at 10 kHz and analysed with pCLAMP 8.0 software (Axon Instruments) and custom Igor Pro (WaveMetrics, Inc., Lake Oswego, OR, USA)/MATLAB (The Mathworks, Inc., Natick, MA, USA) routines. Bipolar tungsten electrodes were placed in the CA3 stratum pyramidale, and a single pulse (50 µs, 5–10 µA) was applied every 15 s in the presence of 20 µM picrotoxin to stimulate pyramidal neurones. In order to apply small electric fields, parallel tungsten electrodes (300 µm interval) were set, about 20 µm above CA3 stratum pyramidale, parallel to the cell layer axis (i.e. vertical to the direction of the apical dendrites of CA3 pyramids). Sinusoidal field stimulation was incessantly applied as background oscillations, the frequency ranging from 5 to 100 Hz (typically 40 Hz). The intensity was adjusted to produce field oscillations comparable to carbachol-induced gamma oscillations in terms of the fluctuation amplitude of electric fields (5 mV mm–1). The amplitude of the imposed field oscillations was decreased as the distance from the parallel electrodes increases; the amplitude was reduced roughly by 70% every 200 µm.
We report the mean ± standard deviation (S.D.) in all measurements.
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Results |
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Visually identified CA3 pyramidal neurones were held in current clamp, and a stimulating electrode was placed in the CA3 pyramidal cell layer about 500 µm from the recording patch-clamp electrode. We found that single-pulse stimuli evoked complex intracellular responses that consisted of multiple EPSPs and occasional action potentials (Fig. 1A). The initial EPSP, presumably monosynaptic, was observed at 4.0 ± 0.8 ms of latency (mean ± S.D., n = 23). The peak amplitude was only 11.7 ± 5.5 mV, which did not reach the spike threshold. The initial response was followed by consecutive EPSPs, which accumulated over time, and eventually led to the firing of action potentials. These late responses are suggestive of recurrent excitation and may represent a memory trace that is involved in production of suprathreshold outputs, i.e. action potentials, with a delay.
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Chronometric spiking behaviours generated by an external oscillator
One of the typical population activities of hippocampal neurones in vivo is gamma rhythmic synchronization (Bragin et al. 1995; Csicsvari et al. 2003). In slice preparations, such periodic activity is usually absent, but it can reliably be induced by carbachol, a muscarinic agonist (Fisahn et al. 1998; Fellous & Sejnowski, 2000). We recorded extracellular field potentials from the slices of the CA3 region, and applied carbachol. We observed no gamma activities before application of carbachol, but the gamma oscillations emerged as a peak in the fast Fourier transform (FFT) power spectrum after application of 20 µM carbachol (Fig. 2A).
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To determine whether background gamma oscillations modulate the recurrent firing activities, we applied single-pulse stimuli in the absence or presence of the external oscillator. In the neurone shown in Fig. 2B, single-pulse stimuli evoked typical late responses in the absence of background gamma oscillations (the control) with the first spike latency being 38.7 ± 9.7 ms. In the presence of background gamma oscillations, the same stimuli, which were applied at the phase of 90 deg of the gamma cycle, significantly delayed the occurrence of the first spike to 157.9 ± 7.0 ms (P < 0.001, Student's t test). When the imposed gamma oscillations were terminated, the latency of the first spikes returned to the control level, 26.4 ± 4.1 ms. That may indicate that field oscillations reversibly modify the readout process of a circuit memory.
We next sought to determine whether the latency of the first spikes is related to the gamma phase at which the stimulus is applied. Interestingly, the latency of the first spikes changed greatly with the phase of the gamma oscillations at which the single-pulse stimuli were applied (Fig. 2C). Contrary to the case of stimuli at 90 deg, the first spike was advanced when the stimulation was applied at the phase of 270 deg compared with the control, but no change was observed for the stimulation at 0 or 180 deg. It seemed that the latency of the spike output from the activated circuit might be predicted from the timing stimuli at the phase of gamma oscillation. The latencies of the initial EPSPs did not show much variance among stimulations at different phases, which were 4.20 ± 0.19, 4.30 ± 0.19, 4.44 ± 0.19, 4.25 ± 0.19 and 4.22 ± 0.19 ms in the control and 0, 90, 180 and 270 deg phases, respectively (see also Fig. 2C traces), but the amplitudes varied depending on the phase at which the stimuli were applied (Fig. 2D). The amplitudes of the initial EPSPs were smallest at the phase of 90 deg and largest at the phase of 270 deg, and they seemed to be responsible for the variation of the first spike latency among stimulations at different phases. The plot of the mean and S.D. of the first spike latencies revealed that in the presence of the imposed gamma oscillations, the S.D. was kept low, regardless of the latencies, indicating that the spike precision was maintained during the signal propagation over hundreds of milliseconds (Fig. 2E). With field oscillations, the circuit is likely to operate with high reliability as if it works as a ‘timer’.
We also examined whether the time when the spike occurs is related to the phase of the gamma oscillations. The times of the first spike occurrence did not seem to be related to the phase of the gamma oscillations (Fig. 1A of the on-line Supplementary Material accompanying this paper). The interspike intervals (ISIs) and the spike numbers were plotted for evaluation of the times of successive spikes following the first spike (Supplementary Fig. 1B). The ISIs were not always locked to a multiple of the gamma cycle (25 ms), but they were sometimes locked to some particular intervals, depending on the case, indicating that the individual timings of discharging spikes after the first spike is not strongly affected by the imposed gamma oscillations but may probably be related to the intrinsic properties of the individual neurones.
Gamma-specific enhancement of recurrent excitation
We next examined the dynamics of the subthreshold membrane potentials to find some mechanism for how the background gamma oscillations affect the recurrent activity. The subthreshold responses were monitored through QX314-loaded patch-clamp electrodes to block action potentials. We found that the gamma field oscillations per se induced small, virtually negligible fluctuations in membrane potential (Fig. 3A, Gamma only), and single-pulse stimuli elicited successive polysynaptic EPSPs following the initial monosynaptic EPSP (Fig. 3A, Stimulus only), but when the background gamma oscillations were applied, the polysynaptic EPSPs occurred more frequently, and their occurrence seemed to be in synchrony with the gamma cycles (Fig. 3A, Stimulus with gamma). The onset times of the individual EPSPs and the phase of the gamma oscillations were plotted for the evaluation of the synchronization (Fig. 3B). The onset times of the recurrent EPSPs were found to be predominantly locked at the phases of 310–360 deg of the gamma oscillations, probably indicating that the synaptic inputs are regulated by the imposed gamma oscillations.
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We next applied background gamma oscillations with different frequencies trying to find the frequency preference in the gamma enhancement. These results and their FFT power spectra are shown in Fig. 3D. Different frequencies of the background gamma oscillations displayed different degrees of synchronization with the polysynaptic EPSPs, which can be more clearly seemed by the peak amplitudes in the FFT power spectra. In the cell shown in Fig. 3D, the highest peak was at 30 Hz, but it varied from cell to cell. By changing the oscillation frequency in the range from 5 to 100 Hz, we did a broad scan frequency preference in the background frequency enhancement (Fig. 3E). The maximal peaks ranged from 28.4 to 36.9 Hz (mean 33.5 ± 3.5 Hz, n = 7 cells), and the width at half-height ranged from 8.0 to 15.8 Hz (mean 12.5 ± 2.6 Hz). Therefore, the enhancement of the background oscillations seemed to show a preference for the gamma-band frequency.
Correlated network operation has been considered to be through NMDA receptors (Lisman et al. 1998; Wang, 1999). Considering this, we applied D,L-AP5, an NMDA receptor antagonist, and found that the later polysynaptic EPSPs, which evoke gamma enhancement, were blocked, but the initial EPSPs were spared (Fig. 4). Both the initial and late responses were abolished by CNQX, a non-NMDA receptor antagonist (Fig. 4). These results suggested that the gamma enhancement is network-based, and depends on NMDA receptor activity.
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Discussion |
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Following an input stimulus, the CA3 circuit displayed a suprathreshold output with a delay that far exceeded a monosynaptic interval. To do this, the circuit has to ‘remember’ a previous transitory stimulus; activity must be present in the circuit until the first spike emerged in a recorded neurone. In this sense, the late spike output represents readout from a memory trace registered in the circuit. Subthreshold membrane potential during the ‘memory’ emerged as accumulating polysynaptic responses. The memory trace is hence likely to depend on local circuit reverberation (Wang, 2001) or attractor dynamics (Durstewitz et al. 2000a), both of which have been theorized to exist in a feedback network such as the CA3 circuit. Consistent with this, blockade of NMDA receptors interfered with evoked polysynaptic responses (Lisman et al. 1998; Wang, 1999).
Under naive conditions, the CA3 memory trace appears unreliable in temporal precision, however. Spike jitter easily expanded as the latency increased, and this nature might limit the cortical function. However, field oscillations are capable of reducing this indeterminacy, stabilizing activity propagation. In addition, the circuit output was precisely timed by input timings relative to the oscillatory phases. Oscillations may ensure accurate decoding of cortical networks by offering an external clock reference. The cellular mechanisms by which spike output was modulated by input phases cannot be deduced from this study alone. Our computational simulation using a layered recurrent network with an inner oscillator and noise replicates similar phase-dependent dynamics of spike modulations (see Supplementary Fig. 2); the result that the modulation range is narrower than that of the real network is probably due to much fewer layers of neurones, but we consider it noteworthy that the phase-dependent dynamics can be mimicked even in the neural networks consisting of only three layers. In this model, synchronization of synaptic transmission was essential for the phase modulation, so it is possible that similar paradigms are implemented in realistic neural networks because our empirical data showed that polysynaptic EPSPs were entrained to the forcing oscillations.
The effect of field oscillations was specific for the gamma-band frequency range. This is intriguing because gamma rhythmic activity is involved in sensory binding (Gray, 1994; Singer, 1999), memory encoding (Fell et al. 2001), attention (Fries et al. 2001), and conscious experience (Varela et al. 2001; Ward, 2003). The CA3 network responses may inherently be optimized to resonate with electric field oscillations only for frequencies in the gamma range. Gamma field oscillations, which alone induced minimal changes in membrane potential of CA3 neurones, facilitated recurrent excitation when an input stimulus was given together. How can gamma field oscillations modulate neural processing only when the circuit is activated? A single-pulse stimulus induced a persistent depolarization shift of membrane potential (a so-called UP state). During the period of a UP state, the neurones are more sensitive to small inputs (Shu et al. 2003; Destexhe et al. 2003). The enhancement of neuronal responsiveness to field oscillations may induce spike synchronization, increasing the temporal reliability (Diesmann et al. 1999). Another, but not exclusive, possibility is synchronization of membrane potential at synapses. The synapses are small structures, and their surface-to-volume ratios are quite high. It is possible therefore that synapses are more susceptible to the surrounding electric field than the soma so that their membrane potential may be subject to synchrony with field oscillations; note that such local oscillations, if any, cannot be detected by whole-cell recordings due to the problem of incomplete ‘space clamp’ (Rall & Segev, 1985; Koch, 1998). If presynaptic membrane potential oscillations are synchronized across synapses, synaptic transmission would also be correlated in time. This is consistent with our observations that polysynaptic EPSPs were synchronized with field oscillatory cycles.
In conclusion, the present study has addressed the effect of field oscillations on temporal processing of the CA3 recurrent circuit and suggests the presence of a novel mode of interneuronal communications mediated by local electric fields, that is, neural synchronization is capable of affecting the spiking behaviours of other neurones. Depending on input timings relative to the gamma cycle, the output latency was coordinated with high reliability, and the shift range (> 100 ms) was several oscillation cycles long, being far longer than the delay of a single-synapse step, which suggests that the input phase alters the trajectory of information flow in the microcircuit. Thus, field oscillations rapidly settle functional cortical architectures into a preferred memory trace in a state-specific manner.
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Supplementary material |
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Supplementary Figure 1. Spike timing relative to ongoing gamma oscillations during persistent depolarization shift
Supplementary Figure 2. Computational confirmation of oscillation-induced modulations of the first spike latency in the layered recurrent neural network
This material can also be found at:http://www.blackwellpublishing.com/products/journals/suppmat/tjp/tjp544/tjp544sm.htm
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