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School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, United Kingdom
Submitted 19 December 2003; accepted in final form 27 February 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Hamill et al. 1981). The whole cell technique is believed to result in less damage to the recorded cell and lead to a more faithful recording of the cell's electrical signals. However, recording from neurons in vivo with patch pipettes has proven to be quite a challenge, and sharp electrode recording is still being used. The advantages and disadvantages of both recording techniques have been extensively compared in single-electrode recordings or computer models (small model neurons, Ince et al. 1986; salamander olfactory neurons, Pongracz et al. 1991; hippocampus neurons, Staley et al. 1992; turtle spinal cord, Svirskis et al. 1997; rat spinal neurons, Thurbon et al. 1998). In some cases in recordings from small neurons, it has been suggested that the effects of recording with sharp electrodes could be so serious that researchers may draw radically different conclusions if the recordings were made with patch pipettes (Aiken et al. 2003; Dale 1995; Dale and Kuenzi 1997). To evaluate these concerns, a direct comparison of the two methods applied to neurons was required. The only previous direct comparison was made on cultured human monocytes (Ince et al. 1986). In this study, we used two electrodes to record simultaneously from single neurons in the developing spinal cord in tadpoles of the frog Xenopus with two types of electrodes. This allowed us to directly compare the recordings made with a patch pipette in whole cell, current-clamp mode to those made with a sharp electrode. We did not carry out a detailed biophysical analysis but evaluated the effects of recording on some particular neuronal properties. Our aim was to see if the recording technique changed the neuron's resting properties or its firing activity both to injected current and during responses evoked by sensory stimulation.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). Xenopus tadpoles at stage 37/38 (see Fig. 1A) were anesthetized with 0.1% MS-222 (3-aminobenzoic acid ester, Sigma, UK) and pinned in a small bath of saline (concentrations in mM: 115 NaCl, 3 KCl, 2 CaCl2, 2.4 NaHCO3, 1 MgCl2, and 10 HEPES, adjusted with 5 M NaOH to pH 7.4). The dorsal fin was cut, and the tadpole was transferred to 10 µM 
-bungarotoxin saline for immobilization (20–30 min). It was re-pinned so that the skin and muscles over the right side of the spinal cord could be removed. A dorsal cut was made along the midline of the spinal cord to open the neurocoel and expose neuronal cell bodies. Some ependymal cells in the neurocoel were cut to expose more ventral neurons. The animal was then re-pinned on a small rotatable Sylgard stage in a 700-µl recording chamber that allowed bright-field illumination from below on an upright Nikon E600FN microscope. The animal was tilted to an angle that allowed partially exposed neuronal cell bodies on the right side of the cord to be seen using a 40x water immersion lens. Saline in the chamber was kept circulating at about 2 ml/min.
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. Fluorescent images were acquired using a Penguin 150 CLM camera (Pixera) with B-2A filter. Sharp electrodes were filled with 3 M KAC and had DC resistances of 150-180 M. Electrodes were pulled on Brown-Flaming pullers (P-87 and P-97, Sutter Instruments) and manipulated with motor driven manipulators (SD Instruments). In each experiment, a whole cell recording in current-clamp mode was made first from the soma (
20 µm diam) to monitor the recording process. The second sharp electrode or patch pipette was brought up against the soma of the same neuron under visual guidance (800x magnification, Fig. 1) for impalement or gigaohm seal formation. A "tearing buzz" of 10 x 2 ms, 5-nA current pulses at 200 Hz was used after the tip of the electrode was pressed against soma membrane to achieve membrane penetration with sharp electrodes and break through after gigaohm seal formation with patch electrodes. Light positive pressure was always applied to the patch pipette solution before trying to get a seal. Each electrode was used only once. A stimulating suction electrode was placed on the tail skin to apply 1-ms current pulses to start fictive swimming activity. Another suction electrode was placed usually on the 11th intermyotome cleft to record ventral root activity during evoked fictive swimming. Signals were recorded with an Axoclamp 2B amplifier in conventional bridge mode. Data were acquired with Signal software through a CED 1401 Plus (CED, Cambridge, UK) with a sampling rate of 10 kHz. Stimuli to the skin were controlled using the CED 1401 Plus configured by Signal and given via an optically coupled isolator. All means are given with their SD unless otherwise stated. Off-line analyses were made with Minitab and Excel. Photos were processed with Adobe Photoshop.
Dual sharp-patch recordings were made from 18 neurons (9 stable) and dual patch-patch recordings from 9 neurons (5 stable). Only those recordings with stable series resistances in the patch electrodes and stable resting membrane potentials (RMPs) in the sharp electrodes were used in the analyses. Stable, dual sharp-patch recordings lasted for 3-15 min. A paired Student's t-test was used to compare means unless stated otherwise. Experiments comply with UK Home Office regulations and have local ethical review approval.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Effects of electrode penetration or breakthrough
As outlined above, the whole recording process for both sharp and patch test electrodes was monitored using a control whole cell patch pipette, applied first and detached last. Penetration of the cell membrane was always difficult with sharp electrodes (Fig. 2, A–C). Very often, applying the tearing buzz only resulted in a small (10–20 mV) negative shift in potential measured by the sharp electrode (Fig. 2A). The control electrode recording showed that these unsuccessful attempts at penetration caused the neuron to fire a burst of spikes followed by sustained depolarization of up to 20 mV. This depolarization may have resulted from an influx of extracellular sodium ions, and recovery to the previous level could take >1 min. Successful penetrations that led to stable recordings (n = 9) often followed a larger initial negative jump in membrane potential in the sharp electrode (Fig. 2B). Sometimes (n = 3/9) the neurons fired a long train of action potentials following the tearing buzz while the membrane potential remained depolarized after the penetration (Fig. 2C). Following sharp electrode penetration, it usually took the membrane potential 1–2 min to reach a new stable level (–55.1 ± 3.2 mV), which was always more positive than the precontrol levels (–62.0 ± 4.9 mV), measured by the control electrode before sharp electrode penetration (P < 0.001, n = 9).
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RMPs and tip potentials
It was immediately clear that the RMPs measured by sharp electrodes differed from those measured by the control electrode. The most likely explanation for this was differences in electrode tip potential. Tip potentials for sharp electrodes and patch pipettes (test and control) were zeroed before each electrode contacted a spinal neuron. After recording and subsequent electrode withdrawal or detachment, strong current pulses and/or brief capacitance overcompensation were used to clear both types of electrode to get a further, stable "final" tip potential reading. For control patch electrodes, tip potential did not change significantly (final difference, 0.5 ± 1.8 mV; range –1.4 to 4.7). However, in nine recordings with sharp test electrodes, final tip potentials changed by –14.0 ± 3.5 mV (range, –9.0 to –18.9 mV). These changes were significantly greater than those for control patch pipettes in the same recordings (P < 0.001) and suggested that sharp electrode measurements of neuronal RMP would be less reliable than those from patch electrodes.
Neuronal RMP measurements were made by taking the difference between the stable membrane potential, measured at a time when there was no obvious synaptic activity like swimming, and the final tip potential. RMPs measured from the control (patch) electrode after sharp electrode penetration were –55.1 ± 3.2 mV, showing that they fell from the precontrol value (–62.0 ± 4.9 mV). As expected from differences in tip potential stability, sharp electrode measurements of RMP differed from these control electrode values during simultaneous recordings. They were rather more negative: –61.4 ± 6.3 mV. We do not consider that there is any completely reliable method for measuring neuronal RMPs. However, the stability of measurements during paired patch electrode recordings make us confident that the reduction in resting potential measured by the control patch electrode following sharp electrode penetration was a real change.
Effects of electrodes on leakage resistance
One of the conclusions drawn in previous studies comparing whole cell and sharp recordings was that penetration with a sharp electrode introduced a significant leakage resistance across the membrane of the recorded cell (Dale 1995; Staley et al. 1992; Svirskis et al. 1997; Thurbon et al. 1998). We therefore used responses to subthreshold current pulses to plot I-V curves (Fig. 3, A and B) and calculate the cellular input resistance (Ri) during different stages of recording. The precontrol Ri for the nine neurons was 846 ± 527 M (range, 262–1,963 M). After the sharp electrode recordings had stabilized, Ris measured with the control patch pipette showed a significant 28.9 ± 11% decrease to 560 ± 275 M (Fig. 3C; n = 9; P = 0.013). Of nine stable, simultaneous sharp-patch recordings, seven survived withdrawal of the sharp electrode. In these neurons, Ris recovered to 89.2 ± 12.9% (827 ± 453 M) of the precontrol measurements (n = 7; P = 0.128). The leakage resistance (Rl) during sharp electrode impalement was calculated as an additional resistance in parallel with the membrane resistance (Rm) using the following equation: Rl–1 = Ri–1 – Rm–1 (where Rm was equal to the value of Ri prior to sharp electrode impalement). Values ranged from 1.31 to 3.32 G (1.95 ± 0.69 G).
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to 502 ± 327 M, n = 5; P = 0.173). It was often difficult to measure the additional leakage resistance in patch-patch recordings because, where Ri was already less than 1 G, the change in Ri was small and similar to the progressive change in series resistance (tens of Ms) that occurred during recordings. Nevertheless, estimates of leakage resistances of the test pipettes in four of five recordings gave relatively consistent values (9.9 ± 3.4 G; range: 4.8-11.7 G). After withdrawal of a test patch pipette, Ri recovered to 96.8 ± 7% (502 ± 329 M) of its initial value (n = 5; P = 0.36). As might be predicted from the relatively high value of the additional leak resistance during sharp electrode recording, the reduction in Ri following sharp electrode impalement was significantly greater for neurons with higher initial Ri than those with a lower Ri (Pearson correlation coefficient = 0.817, P = 0.007, Fig. 3D). Because of the much smaller change of Ri, a similar relationship was not obvious in patch-patch recordings (coefficient = 0.615, P = 0.269). The leak resistances were not correlated to initial Ri in either type of recordings (P = 0.197 for sharp-patch and P = 0.279 for patch-patch recordings).
Effects of recording on neuronal firing to current injection
It has been predicted that a consequence of the shunting effect of sharp electrode impalement will be a qualitative change in the firing properties of neurons (Dale 1995). We therefore looked at firing responses of neurons to depolarizing current injection. Since sharp electrode penetration led to a drop in Ri, the positive current needed to make neurons fire might be expected to increase after sharp electrode penetration. However, the RMP also became more positive during sharp electrode recording. Possibly as a result of this depolarization, the smallest current needed to make neurons fire spikes did not change significantly (from 94 ± 87 to 83 ± 69 pA, n = 7, P = 0.245). Before recording with the test electrode (sharp or patch), the 16 neurons recorded showed a range of firing responses to depolarizing current. These could be divided qualitatively into four main categories: a single spike only (n = 1), a brief burst of 
6 spikes (n = 2), a train of spikes (Fig. 4A; n = 10), or a delayed train usually following a single spike (Fig. 4B; n = 3). In all seven cases where the test electrode was a second patch electrode, there was no qualitative change in the pattern of response (data not shown). In seven of the nine sharp electrode impalements, there was again no qualitative change in firing responses (Fig. 4). In the other two cases, there was a partial change: one from brief bursts to trains and the other from trains to brief bursts. There was usually a small quantitative change; firing frequencies to a given current were altered: sometimes increased and sometimes decreased (Fig. 4, C and D).
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Effects of recording method on spiking activity during fictive motor responses
To assess the effects of the recording technique on the normal activity of spinal neurons, we looked at eight neurons showing clear synaptic activity during fictive swimming, evoked when the tail skin was stimulated with a 1-ms electrical pulse (cf. Li et al. 2002). Before going whole cell with the control patch electrode, we recorded activity in cell-attached mode (n = 8). These extracellular recordings provide the best available control of the normal pattern of firing activity for individual neurons during swimming: because the neuron membrane remains intact, trans-membrane chemical gradients will therefore not be perturbed as in either whole cell mode or sharp electrode intracellular mode.
We have shown previously that the whole cell recording does not change the firing pattern of neurons during swimming (Li et al. 2002). We now asked whether neurons tended to fire less reliably after test electrode (sharp or patch) penetration. Of the eight neurons recorded, five were sensory interneurons, which only fired action potentials shortly after skin stimulation before swimming started (Clarke and Roberts 1984; Li et al. 2003; Sillar and Roberts 1988), and three were premotor neurons, which fired rhythmically during swimming. During simultaneous sharp-patch recording, the pattern of neuron firing following skin stimulation or during swimming appeared to remain unchanged throughout the whole recording processes (Fig. 5A). The reliability of firing was tested in sensory interneurons by counting the number of spikes to a series of >10 equal-strength skin stimuli, or, in CPG neurons, by measuring the percentage of swimming cycles with spikes in >200 cycles at equivalent frequencies. When these measures were compared in four sensory pathway interneurons and three CPG neurons before and after sharp electrode penetration, firing reliability was not changed significantly (F test, P > 0.05). In the remaining sensory interneuron, firing reliability was increased (F test, P < 0.05). Similar results were observed where the second, test electrode was a patch pipette (n = 5 CPG neurons; data not shown). These results suggest that sharp electrodes give as accurate a picture of firing patterns during fictive motor responses such as swimming as whole cell patch electrodes.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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), but once obtained, have often been stable for long periods (>60 min) (Soffe and Roberts 1982). Our present methods allow simultaneous whole cell and sharp electrode recording from the somata of single spinal neurons that can be seen at 800x magnification with bright-field illumination after the spinal cord is opened along the dorsal midline (Li et al. 2002, 2003). This has made it possible for us to examine the effects of sharp electrode recording directly.
By monitoring the whole recording process with our control whole cell patch electrode, we were able to judge the extent to which a further sharp or patch electrode penetration altered the neuron's properties and responses. Going whole cell with a second patch electrode led to very little change, but sharp electrode penetration led to depolarization (Ince et al. 1986), sometimes with injury discharge. The RMP could take minutes to recover and stabilize. The membrane damage produced by the sharp electrodes was measured as a 20–40% drop in input resistance compared with an insignificant drop of 0.8–6.6% with a patch electrode. The effect of the shunt or leakage resistance (1.3–2.6 G) introduced by the sharp electrode appeared to be larger in neurons with higher Ri, which are presumably smaller. These results give direct support for earlier studies that often used models of recorded neurons and concluded from sequential comparison of sharp and whole cell recordings that the sharp recordings caused a leakage resistance to appear in the neuron membrane (Cymbalyuk et al. 2002; Dale 1995; Staley et al. 1992; Svirskis et al. 1997; Thurbon et al. 1998). It has been pointed out (Jack 1979; Pongracz et al. 1991) that the leakage introduced by sharp electrodes may be trivial in large mammal motoneurons with low Ri (0.6 M) but is likely to be significant in smaller neurons with high Ri such as those in the olfactory bulb (2–5 G) or tadpole spinal cord (0.2–2 G; this study).
Other problems associated with sharp electrode recordings from smaller neurons come from the need to use fine electrodes with high resistances (150–180 M) to obtain stable recordings. While tip potential and capacitance can be compensated before recording, there can be no certainty that these properties do not change when the electrode tip is inside the neuron. Large tip potentials have to reduce confidence in measures of resting potentials with sharp electrodes, but there may also be problems with low-resistance whole cell patch recordings (Verheugen et al. 1999). In both cases, the pipette solution is in contact with the cell interior, so dialysis may alter cytoplasm ionic composition and in this way change the resting potential. The effects of inadequate compensation for the capacitance of fine sharp electrodes is another problem that became obvious during simultaneous sharp-patch recordings of spiking activity (Fig. 4). The overshooting impulses recorded by the whole cell electrode were recorded at a much lower, often non-overshooting, amplitude by the sharp electrode. Although the reduced spike height could have been due to a leakage resistance (Dale 1995), these recordings show that large spikes are still present after sharp electrode penetration, suggesting that they are attenuated by the low-pass filtering of the sharp electrode, rather than by damage. Despite following "standard practice," where the frequency response of sharp electrodes appeared adequate before impalement, our results show that capacitance neutralization was clearly not adequately achieved during impalement.
If sharp electrodes produce a 20–40% drop in neuron input resistance, one might expect the neuron's firing properties and activity following sensory stimulation to be changed. We compared recordings of responses to skin stimulation after penetration with a second sharp or patch electrode and did not observe any consistent differences. As for firing properties, it has been argued that damage during sharp electrode recording leads to Xenopus tadpole spinal neurons being less excitable and only firing once to current injection (Aiken et al. 2003; Dale 1995). However, some neurons recorded with sharp electrodes can fire repetitively to depolarizing current (Roberts and Sillar 1990; Soffe 1990), and some neurons recorded with whole cell patch electrodes only fire single impulses (Dale 1991). When we looked at the firing responses of neurons to injected current, we found a number of different firing patterns from single spikes to trains, such as those described recently by Aiken et al. (2003) and in our own large sample of single patch-electrode recordings (unpublished data). After sharp-electrode penetration, slightly more current was required to evoke the same pattern of spikes, but apart from this, the neurons' firing responses appeared to be largely unchanged. Observations of firing activity recorded using the two types of electrode from the same neurons give us confidence that the firing activity described on the basis of sharp electrode recordings from many types of smaller neuron may be valid.
Does any discrepancy still exist over reported firing patterns in Xenopus tadpole spinal neurons? There is clearly agreement that neurons active during swimming and recorded with whole cell patch electrodes can show repetitive firing to injected current (Fig. 4; Aiken et al. 2003; Li et al. 2002). Since we have concluded that sharp electrode recordings give a reliable record of firing activity, we would predict that patch recordings, like earlier sharp electrode recordings (Soffe 1990), would reveal more ventral neurons that fire only once to injected current. From our estimates of the degree of membrane shunting following sharp electrode impalement and earlier sharp electrode measurements of input resistance, we also predict that they have relatively low input resistances. It may be that Aiken et al. (2003) did not describe such single impulse firing either because of the greater difficulty of recording more ventral neurons with patch electrodes or because they rejected all recordings with input resistances <500 M. Further recordings will be required to resolve this issue.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: W.-C. Li, School of Biological Sciences, Univ. of Bristol, Woodland Rd., Bristol BS8 1UG, UK (E-mail: wenchang.li{at}bristol.ac.uk).
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Clarke JDW and Roberts A. Interneurones in the Xenopus embryo spinal cord: sensory excitation and activity during swimming. J Physiol 354: 345–362, 1984.
Cymbalyuk GS, Gaudry Q, Masino MA, and Calabrese RL. Bursting in leech heart interneurons: cell-autonomous and network-based mechanisms. J Neurosci 22: 10580–10592, 2002.
Dale N. The isolation and identification of spinal neurons that control movement in the Xenopus embryo. Eur J Neurosci 3: 1025–1035, 1991.[CrossRef][Web of Science][Medline]
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Dale N and Kuenzi FM. Ion channels and the control of swimming in the Xenopus embryo. Prog Neurobiol 53: 729–756, 1997.[CrossRef][Web of Science][Medline]
Fenwick EM, Marty A, and Neher E. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol 331: 577–597, 1982.
Hamill OP, Marty A, Neher E, Sakmann B, and Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch 391: 85–100, 1981.[CrossRef][Web of Science][Medline]
Ince C, van Bavel E, van Duijn B, Donkersloot K, Coremans A, Ypey DL, and Verveen AA. Intracellular microelectrode measurements in small cells evaluated with the patch clamp technique. Biophys J 50: 1203–1209, 1986.[Web of Science][Medline]
Jack JJB. An introduction to linear cable theory. In: The Neurosciences: Fourth Study Program, edited by Schmitt FO and Worden FG. Cambridge, MA: MIT Press, 1979, p. 423–437.
Li WC, Soffe SR, and Roberts A. Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci 22: 10924–10934, 2002.
Li WC, Soffe SR, and Roberts A. The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex. J Neurosci 23: 9068–9077, 2003.
Pongracz F, Firestein S, and Shepherd GM. Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. J Neurophysiol 65: 747–758, 1991.
Roberts A and Sillar KT. Characterization and function of spinal excitatory interneurons with commissural projections in Xenopus laevis embryos. Eur J Neurosci 2: 1051–1062, 1990.[CrossRef][Web of Science][Medline]
Sillar KT and Roberts A. Unmyelinated cutaneous afferent neurons activate two types of excitatory amino acid receptor in the spinal cord of Xenopus laevis embryos. J Neurosci 8: 1350–1360, 1988.[Abstract]
Soffe SR. Active and passive membrane properties of spinal cord neurons that are rhythmically active during swimming in Xenopus embryos. Eur J Neurosci 2: 1–10, 1990.[CrossRef][Web of Science][Medline]
Soffe SR and Roberts A. Tonic and phasic synaptic input to spinal cord motoneurons during fictive locomotion in frog embryos. J Neurophysiol 48: 1279–1288, 1982.
Staley KJ, Otis TS, and Mody I. Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J Neurophysiol 67: 1346–1358, 1992.
Svirskis G, Gutman A, and Hounsgaard J. Detection of a membrane shunt by DC field polarization during intracellular and whole cell recording. J Neurophysiol 77: 579–586, 1997.
Thurbon D, Luscher HR, Hofstetter T, and Redman SJ. Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol 79: 2485–2502, 1998.
Verheugen JA, Fricker D, and Miles R. Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19: 2546–2555, 1999.
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