John M. Walker, SERIES EDITOR 288. Patch-Clamp Methods and Protocols, edited by Peter Molnar and James J. Hickman, 2007 399. Neuroprotection Methods and Protocols, edited by Tiziana Borsello, 2007 286. Transgenic Plants: Methods and Protocols, edited by Leandro Peña, 2004 285. Cell Cycle Control and Dysregulation Protocols: Cyclins, Cyclin-Dependent Kinases, and Other Factors, edited by Antonio Giordano and Gaetano Romano, 2004 284. Signal Transduction Protocols, Second Edition, edited by Robert C. Dickson and Michael D. Mendenhall, 2004 283. Biconjugation Protocols, edited by Christof M. Niemeyer, 2004 282. Apoptosis Methods and Protocols, edited by Hugh J. M. Brady, 2004 281. Checkpoint Controls and Cancer, Volume 2: Activation and Regulation Protocols, edited by Axel H. Schönthal, 2004 280. Checkpoint Controls and Cancer, Volume 1: Reviews and Model Systems, edited by Axel H. Schönthal, 2004 279.
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Rhythmic stimulation of fornix/fimbria evoked IPSPs, which significantly activated putative GABAergic neurons of the MS/DB. A, Effect of fornix stimulation (stim) on electrophysiologically identified MS/DB neurons. Compared with baseline level (bsl), the firing of fast- and burst-firing neurons was dramatically increased during rhythmically evoked IPSPs, whereas that of slow- and cluster-firing cells was not changed. Error bars represent SEM (***p < 0/001). B, C, Phase-firing pattern of fast- and burst-firing neurons during rhythmic stimulation of the fornix. The phase histograms show that both fast- and burst-firing neurons exhibit maximal discharge probability just before the following stimulation in each cycle consistent with rebound activation. A Gaussian fit is shown for both distribution (solid gray line), and a dashed vertical line marks the point of stimulation (360°).
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Figure 4A shows the proportion of rebound spikes per IPSPs for the four different types of MS/DB neurons. Burst-firing cells showed the highest proportion of IPSPs with rebound spikes, whereas fast-firing cells displayed a slightly lower amount. In contrast, most slow-firing (cholinergic) and cluster-firing neurons had no rebound spikes or, when present, the lowest number of spikes per IPSPs. The fact that fast- and burst-firing MS/DB neurons fired consistently on the rebound from IPSPs suggested that, paradoxically, hippocampal inhibition may lead to an activation of these two cell types. To investigate this phenomenon in more detail, we specifically examined the firing of MS/DB neurons during the peak of carbachol-induced hippocampal activity by comparing firing frequency during control (1 min) and carbachol peak activity (20 s).
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The electrodes were lowered into the tissue in or near the pyramidal layer. In control experiments with the isolated intact hippocampus, field recording electrodes were filled with pontamine sky blue (PSB) (2% in 0/5 m NaCl), and PSB was injected iontophoretically (10 μA) at the end of the session to localize the recording site. Recordings were performed using a BVC-700A amplifier (Dagan, Minneapolis, MN) equipped with an AC-coupled extracellular Headstage (model 8024) with a 1000 × Vm gain and a low-cut filter set at 0/3 Hz.
The voltage-clamp protocols used in this study were designed to efficiently probe the kinetics of all ion channel types considered here (Hodgkin and Huxley, 1952b; Willms et al, 1999; Ranjan et al, 2021). Measuring the kinetic responses of each channel model allowed us to compare models regardless of their specific implementation. Notably, our method (check here) is amenable to the addition of other protocols that may be better suited to separate certain models. However, there is evidence that simple step and ramp current pulses are sufficient to probe the underlying kinetics of neurons (Druckmann et al, 2021), similar to the voltage-clamp protocols that we use here. Additionally, the simplicity of our protocols makes experimental comparison easier.
Indeed, fast-firing neurons fired immediately before the peak (mean 331°; n = 4), whereas burst-firing neurons tended to fire more often between cycles (mean 250°; n = 8), indicating that the hippocamposeptal inhibitory input could contribute to differential timing of MS/DB neurons firing. Together, these results suggest that hippocampal inhibition may represent a powerful mechanism for selectively activating and synchronizing large populations of cells in the MS/DB.
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Effect of the Ih current blocker ZD 7288 (ZD) on rebound spiking of MS/DB neurons. A, Trains of electrical stimulation (Stim) to the fornix/fimbria reliably evoked rhythmic IPSPs and rebound spikes in an MS/DB burst-firing neuron during control recording (ACSF perfusion). B, C, In contrast, at 15 min after addition of ZD to the bath perfusion (B), rebound spikes were much sparser, whereas at 30 min (C), they were no longer present, although IPSPs could still be evoked.
The medial septum diagonal band area (MS/DB) is a key generator of 3–12 Hz theta oscillations in the hippocampus (Buzsaki, 2002), and theta activity of hippocampal neurons is implicated in spatial cognition, memory processes, and sensorimotor integration (Winson, 1978; Bland and Oddie, 2001; Buzsaki, 2002). Although how the MS/DB generates hippocampal theta is incompletely understood, the current model suggests that MS/DB cholinergic (ACh) and GABAergic neurons have distinct roles. MS/DB ACh neurons may convey a sustained depolarization of hippocampal neurons, whereas MS/DB GABAergic neurons rhythmically inhibit hippocampal GABAergic interneurons, which in turn pace pyramidal neurons (Freund and Antal, 1988; Toth et al, 1997). A role in theta for the recently described glutamate neurons in the MS/DB still remains to be determined (Sotty et al, 2003; Manseau et al, 2005; Colom et al, 2005). Conversely, the hippocampus is known to have important projections back to the MS/DB (Alonso and Kohler, 1982; Toth et al, 1993). The input from hippocampus to septum originates principally from GABAergic neurons located in st. oriens of CA1/CA3 (Toth et al, 1993; Gulyas et al, 2003). These hippocamposeptal projecting GABA neurons are innervated by local CA1/3 pyramidal neurons and are therefore critically situated to transmit rhythmic activity to the septum (Blasco-Ibanez and Freund, 1995). Hippocamposeptal GABA neurons synapse preferentially in the MS/DB on GABAergic neurons but also to a lesser extent on ACh neurons (Toth et al, 1993). In contrast, CA1/CA3 pyramidal neurons may directly innervate only neurons of the lateral septum, which are sparsely connected to the MS/DB (Leranth et al, 1992; Linke et al, 1995). The inhibitory hippocamposeptal pathway is therefore considered the only monosynaptic hippocampal connection back to the MS/DB.
The medial septum diagonal band area (MS/DB) projects to the hippocampus through the fornix/fimbria pathway and is implicated in generating hippocampal theta oscillations. The hippocampus also projects back to the MS/DB, but very little is known functionally about this input. Here, we investigated the physiological role of hippocamposeptal feedback to the MS/DB in a complete in vitro septohippocampal preparation containing the intact interconnecting fornix/fimbria pathway. We demonstrated that carbachol-induced rhythmic theta-like hippocampal oscillations recorded extracellularly were synchronized with powerful rhythmic IPSPs in whole-cell recorded MS/DB neurons. Interestingly, we found that these IPSPs evoked rebound spiking in GABAergic MS/DB neurons. In contrast, putative cholinergic and glutamatergic MS/DB neurons responded only weakly with rebound spiking and, as a result, were mostly silent during theta-like oscillations. We next determined the mechanism underlying the rebound spiking that followed the IPSPs in MS/DB GABAergic neurons using phasic electrical stimulation of the fornix/fimbria pathway. We demonstrate that the increased rebound spiking was attributable to the activation of Ih current, because it was significantly reduced by low concentrations of the Ih antagonist ZD7288 [4-(N-ethyl-N-phenylamino)-1,2-dimethyl-6-(methylamino) pyridinium chloride]. Together, these results suggest that rhythmical activity in hippocampus is transferred to the MS/DB and can preferentially phase the spiking of GABAergic MS/DB neurons because of their significant expression of Ih currents. Our data demonstrate that hippocamposeptal inhibition facilitates theta rhythmic discharges in MS/DB GABAergic neurons while favoring the inhibition of most ACh and glutamate neurons.
This book takes a comprehensive approach to addressing these often challenging clinical diagnoses. In particular, it focuses on the two most common of childhood neurodevelopmental disabilities: global developmental delay and developmental language impairment. It seeks to put forward our present conceptualization of these entities as well as their proper evaluation and assessment and diagnosis from a variety of perspectives. It also provides details on our current understanding of the scientific basis of these disorders and their underlying causes. Issues related to medical management, rehabilitation, and eventual outcomes are also addressed in a detailed way. The book has wide appeal to those in paediatrics, developmental paediatrics, child neurology, and paediatric rehabilitation. Its geographic appeal includes both developed and developing nations as some chapters are devoted to the particular issues faced in underdeveloped countries. The book's focus on both clinical and scientific aspects is invaluable in this field.
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Methods in Molecular Biology
It has been reported that MS/DB neurons in vivo fire bursts of action potentials either in or out of phase with the hippocampal theta rhythm (Stewart and Fox, 1989), a phenomenon recently found to be prominent for GABAergic MS/DB neurons (Borhegyi et al, 2004; Simon et al, 2006). We therefore investigated whether the hippocamposeptal inhibitory input could contribute to the distinct phase preferences of MS/DB neurons.
Here, we explore the K+-conducting function of the mitoBK channel protein in mitochondria isolated from NRK cells for the first time and evaluate the impact of CS+RW on mitoBK channel-mediated K+ uptake. Our attempts to directly assess mitoBK currents using patch-clamp methods in NRK cell mitoplasts were unsuccessful. Instead, we used the cell-permeant K+-binding fluorescent probe PBFI-AM and BK channel modulators to detect changes in [K+]mito, thereby providing a surrogate measurement to evaluate K+ uptake across the mitochondrial membrane. Our protocol (have a peek here) was adapted from Aon et al. who first demonstrated the use of PBFI to measure mitochondrial K+ uptake mediated through mitoBK channels .
We found that IPSPs elicited in the slow and fast groups appeared to have more rapid onsets (30/5 ± 9/4 ms, n = 5 and 51/5 ± 16/5 ms, n = 6, respectively) than those in the burst or cluster groups (53/2 + 7/5 ms, n = 20 and 62/2 + 15/8 ms, n = 9, respectively). No statistical significance was noted between the onsets of the four groups.
Of 46 MS/DB neurons recorded during carbachol-induced rhythmic hippocampal activity, 29 neurons (63%) responded to hippocampal activity with synchronized synaptic potentials. Of those cells, 18 neurons (56%) showed only IPSPs, whereas the remaining 11 neurons (35%) received a mixture of prominent IPSPs and smaller EPSPs. All IPSPs in MS/DB followed the field recorded activity in hippocampus, suggesting that the inhibition was caused directly by hippocampal GABAergic input.
Fast-firing cells typically fired tonically during subthreshold depolarization. Burst-firing neurons displayed higher FMAX values and stronger spike frequency accommodation and produced prominent rebound bursts after hyperpolarizing current pulses. Finally, (4) cluster-firing neurons, which have been identified previously as glutamate neurons within the MS/DB (Sotty et al, 2003), displayed clusters of closely spaced action potentials separated by short intervals of subthreshold membrane oscillations during long-lasting depolarizations. A minority of cells could not be identified clearly using these criteria, because they showed mixed properties and were therefore not included in statistics. Table 1 summarizes the properties of cells belonging to the four main groups.
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Differential activation and phase locking of identified MS/DB neurons during carbachol-induced hippocampal rhythmic oscillations. A, B, Bar graph showing the proportion of IPSPs followed by rebound spiking during peak CCH-induced activity (A) and the increase in firing frequency compared with control ACSF condition for the four types of MS/DB neurons (B). Error bars represent SEM (*p < 0/05). C, D, Phase relationship between hippocampal rhythmic field activity and the spiking of fast-firing (C) and burst-firing (D) neurons of the MS/DB. The average probability of discharge for the two different types of neurons is shown as phase histograms (20 bins/cycles; dark gray bars), whereas smoothed averaged curves (colored lines) were used to illustrate the firing phase of individual neurons. All fast-firing neurons recorded in the dual-chamber experiment fired rebound spikes near the peak (360°) of hippocampal field events. The phase measured at the peak of the average Gaussian fit was 331°. In contrast, most burst-firing neurons tended to fire action potentials at counter-phase from the hippocampal oscillation (mean phase, 250°).
Short Protocols in Neuroscience
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We next went back to examine the mechanisms underlying the apparently paradoxical activation of MS/DB neurons by hippocampal inhibition. Because the carbachol-induced rhythmic activity of the hippocampus was transient and variable, it was not possible to perform adequate pharmacological manipulations in these conditions.
Electrical stimulation of hippocampal GABAergic projections to the septum effectively drives rhythmic bursting activity in MS/DB neurons. A, Schematic diagram showing the septohippocampal preparation with placement of the stimulation electrode in the fornix-fimbria bundle (Stim fornix). B, Recording from a burst-firing cell in which brief stimulation trains (5 pulses of 2 ms; 10 ms ISI) delivered repeatedly to the fornix evoked short-latency IPSPs followed by rebound action potentials when the cell holding potential was depolarized. IPSPs were reduced, and no EPSPs were visible when the membrane potential was held at more negative values with tonic current injection. C, Uninterrupted recording from another burst-firing cell illustrating the protocol used to test the effect of rhythmically evoked IPSPs on the firing of MS/DB neurons. After a baseline period (1 min) at a membrane potential near threshold, a prolonged train of stimulation was applied to the fornix, which evoked large IPSPs leading to an increased firing rate. Di–Diii, Superimposed traces (five times, 10 s recording episodes) showing spike and synaptic activity in a fast-firing MS/DB cell during baseline (bsl) condition (Di), electrical stimulation of the fornix with trains at 2 Hz (Stim) (Dii), and the same stimulation protocol applied in the presence of bicuculline (Bic) (Diii). Notice that evoked rhythmic IPSPs elicit rebound spikes increasing the firing rate (compared with baseline) at phase-locked intervals and that both evoked IPSPs and rebound spiking are abolished after bicuculline (Bic). The membrane potential of this cell was held at a value just above its firing threshold (−47 mV; determined at the start of experiment). E, Spike-triggered average from 10 consecutive evoked IPSPs in ACSF and after addition of bicuculline.
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Note that histogram peaks are distributed at regular intervals, indicating rhythmicity of septohippocam pal activity, and that IPSPs are clustered near the peak of hippocampal field events for fast, burst, and cluster-firing cells. As observed in the distribution histograms, spikes are phase locked to the rebounds of the IPSPs for fast- and bust-firing MS/DB neurons. Hyperpolarization of the holding potential with current injection in the burst-firing cell reduces the amplitude of IPSPs (C, bottom blue trace) and shows the absence of EPSPs, which could contribute to firing. In the slow-firing (A) and cluster-firing (B) cells illustrated, IPSPs are less synchronized with fields and do not generate rebound action potentials. All histograms were built from ∼30 s of recordings during the peak of rhythmic septohippocampal activity.
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Synaptic plasticity, the cellular correlate for learning and memory, involves a number of molecules that reside in the dendritic spine. For example, long-term potentiation (LTP) of the excitatory postsynaptic current (EPSC) is induced by postsynaptic NMDA receptor and Ca 2+ /calmodulin-dependent kinase II (CaMKII) activity.
For all voltage recordings (patch and field), signals were continuously low-pass filtered on-line at 1–2 kHz and sampled at 10–20 kHz using pClamp (9 and 10) software (Molecular Devices, Sunnyvale, CA). Traces were additionally filtered off-line for analysis and presentation. Recorded membrane potentials were not corrected for junction potentials (estimated at −14/4 mV).
Our results suggest that GABAergic MS/DB neurons are specially entrained by the rhythmic inhibitory activity from hippocampus. Although these results were obtained when hippocampal oscillations were in the low range of theta frequency (3–5 Hz), it remains to be determined whether higher-frequency theta activity (6–12 Hz) can produce similar responses in MS/DB neurons. Moreover, it also remains to be established whether carbachol-evoked hippocampal rhythmic oscillations near theta frequency are similar to theta oscillations in vivo (Buzsaki, 2002). Although many have shown theta-like activity using carbachol in slices (Konopacki et al, 1987; Bland and Oddie, 2001), others have suggested that carbachol can elicit hippocampal activity that has some resemblance to epileptiform firing (Williams and Kauer, 1997). However, under our conditions using the septohippocampal preparation, carbachol elicited repetitive oscillatory activity in hippocampus that was clearly nonepileptiform.
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Carbachol infusion in the hippocampus induces rhythmic and synchronized septohippocampal activity. A, Low-magnification picture showing the intact septohippocampal preparation in the dual-bath recording chamber and placement of the electrodes. This configuration allowed independent perfusion of the hippocampal compartment (left) with either ACSF or ACSF plus CCH, whereas the septum side (right) was continuously perfused in normal ACSF during concomitant hippocampal field and MS/DB patch (official site) recordings. The extracellular field electrode was placed in CA3, and the patch (https://aprel-vologda.ru/hack/?patch=5028) electrode was descended through the MS/DB region. In this preparation, the MS and DBs are readily identifiable by their location with respect to the anterior commissur (ac). B, Typical example of simultaneous recording from an MS/DB neuron (whole-cell, current-clamp (click for source); top trace) and from the hippocampus (extracellular field; bottom trace) in the intact septohippocampal preparation. During ASCF perfusion to both hippocampus and septum (left), the MS/DB neuron shows only random discharge and synaptic activity when held at a membrane potential near its firing threshold. After addition of CCH (30 μm; right) to the hippocampal side of the chamber, large rhythmic field potentials appear in CA3, which are synchronized with prominent IPSPs and rebound firing in the recorded MS/DB neuron. Note the increased firing rate of the MS/DB neuron during the hippocampal rhythm. Expanded traces from the CCH-induced response are shown below at two different time scales.
The framework can also be used for the comparison of experimental data and models. To illustrate, we uploaded and tested an experimental dataset of recordings from Kenyon cells in Drosophila melanogaster. Voltage-gated cationic currents across the membranes of these neurons are thought to be dominated by A-type K+ channels, in particular Shal/Kv4 (Gasque et al, 2005). This renders Kenyon cells a suitable neuronal cell type to test the biological relevance of our voltage-clamp protocols in an in vivo setting. Current responses were recorded in targeted whole-cell patch clamp (https://aprel-vologda.ru/hack/?patch=290) experiments in vivo (see Materials and methods (resources)). The recordings were performed using our five standardized voltage-clamp protocols, allowing us to transform and compare the experiments directly to ion channel models in the same ’score’ space (Figure 6C). The comparison revealed a close match to an existing model from our resource, and thus characterizes the behavior of the ion channel as similar to a mammalian Kv4 ion channel (Figure 6C; Fineberg et al. (2021); Kv4_csi, ModelDB ID no. 145672).