PIP2-Mediated HCN3 Channel Gating Is Crucial for Rhythmic Burst Firing in Thalamic Intergeniculate Leaflet Neurons

Lo, Fu-Sun, R. John Cork, and R. Ranney Mize. Physiological properties of neurons in the optic layer of the rat's superior colliculus. J. Neurophysiol. 80: 331–343, 1998. We made intracellular recordings from 74 neurons in the optic layer of the rat superior colliculus (SC). Resting membrane potentials were −62.3 ± 6.2 (SD) mV, and input resistances were 37.9 ± 10.1 MΩ. Optic layer neurons had large sodium spikes (74.2 ± 12.3 mV) with an overshoot of 12 mV and a half-amplitude duration of 0.75 ± 0.2 ms. Each sodium spike was followed by two afterhyperpolarizations (AHPs), one of short duration and one of longer duration, which were mediated by tetraethylammonium (TEA)-sensitive ( I C) or apamin-sensitive ( I AHP) calcium-activated potassium currents, respectively. Sodium spikes were also followed by an afterdepolarization (ADP), which was only revealed when the AHPs were blocked by TEA or apamin. In response to hyperpolarizing current pulses, optic layer neurons showed an inward rectification mediated by H channels. At the break of the current pulse, there was a rebound low-threshold spike (LTS) with a short duration of <25 ms. The LTS usually induced two sodium spikes (doublet). Most optic layer neurons (84%) behaved as intrinsically bursting cells. They responded to suprathreshold depolarization with an initial burst (or doublet) followed by a train of regular single spikes. The remaining 16% of cells acted as chattering cells with high-frequency gamma (20–80 Hz) rhythmic burst firing within a narrow range of depolarized potentials. The interburst frequency was voltage dependent and also time dependent, i.e., showed frequency adaptation. Unmasking the ADP with either TEA or apamin converted all of the tested intrinsically bursting cells into chattering cells, indicating that the ADP played a crucial role in the generation of rhythmic burst firing. Optic layer neurons receive direct retinal excitation mediated by both N-methyl-d-aspartate (NMDA) and non-NMDA receptors. Optic tract (OT) stimulation also led to γ-aminobutyric acid-A (GABAA) receptor–mediated inhibition, the main effect of which was to curtail the excitatory response to retinal inputs by shunting the excitatory postsynaptic current. Intracellular staining with biocytin showed that the optic layer neurons that we recorded from were mostly either wide-field vertical neurons or other cells with predominately superficially projecting dendrites. These cells were similar to calbindin immunoreactive cells seen in the optic layer. The characteristics of these optic layer neurons, such as prominent AHPs, strong shunting effect of inhibition, and short-lasting LTS, suggest that they respond transiently to retinal inputs. This is consistent with a function for these cells as the first relay station in the extrageniculate visual pathway.

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Propofol block ofIhcontributes to the suppression of neuronal excitability and rhythmic burst firing in thalamocortical neurons

European Journal of Neuroscience ◽

10.1111/j.1460-9568.2006.04765.x ◽

2006 ◽

Vol 23 (5) ◽

pp. 1403-1403

Author(s):

Shui-Wang Ying ◽

Syed Y. Abbas ◽

Neil L. Harrison ◽

Peter A. Goldstein

Keyword(s):

Neuronal Excitability ◽

Burst Firing ◽

Rhythmic Burst

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Medial vestibular nucleus in the guinea-pig: apamin-induced rhythmic burst firing — an in vitro and in vivo study

Experimental Brain Research ◽

10.1007/bf00229780 ◽

1993 ◽

Vol 95 (2) ◽

pp. 213-222 ◽

Cited By ~ 38

Author(s):

C. de Waele ◽

M. Serafin ◽

A. Khateb ◽

T. Yabe ◽

P. P. Vidal ◽

...

Keyword(s):

Guinea Pig ◽

Vestibular Nucleus ◽

Burst Firing ◽

In Vivo Study ◽

Medial Vestibular Nucleus ◽

Rhythmic Burst

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Theta-rhythmic drive between medial septum and hippocampus in slow-wave sleep and microarousal: a Granger causality analysis

Journal of Neurophysiology ◽

10.1152/jn.00542.2015 ◽

2015 ◽

Vol 114 (5) ◽

pp. 2797-2803 ◽

Cited By ~ 12

Author(s):

D. Kang ◽

M. Ding ◽

I. Topchiy ◽

L. Shifflett ◽

B. Kocsis

Keyword(s):

Granger Causality ◽

Slow Wave ◽

Rem Sleep ◽

Slow Wave Sleep ◽

Power Spectra ◽

Medial Septum ◽

Burst Firing ◽

Theta Oscillations ◽

Interaction Patterns ◽

Rhythmic Burst

Medial septum (MS) plays a critical role in controlling the electrical activity of the hippocampus (HIPP). In particular, theta-rhythmic burst firing of MS neurons is thought to drive lasting HIPP theta oscillations in rats during waking motor activity and REM sleep. Less is known about MS-HIPP interactions in nontheta states such as non-REM sleep, in which HIPP theta oscillations are absent but theta-rhythmic burst firing in subsets of MS neurons is preserved. The present study used Granger causality (GC) to examine the interaction patterns between MS and HIPP in slow-wave sleep (SWS, a nontheta state) and during its short interruptions called microarousals (a transient theta state). We found that during SWS, while GC revealed a unidirectional MS→HIPP influence over a wide frequency band (2–12 Hz, maximum: ∼8 Hz), there was no theta peak in the hippocampal power spectra, indicating a lack of theta activity in HIPP. In contrast, during microarousals, theta peaks were seen in both MS and HIPP power spectra and were accompanied by bidirectional GC with MS→HIPP and HIPP→MS theta drives being of equal magnitude. Thus GC in a nontheta state (SWS) vs. a theta state (microarousal) primarily differed in the level of HIPP→MS. The present findings suggest a modification of our understanding of the role of MS as the theta generator in two regards. First, a MS→HIPP theta drive does not necessarily induce theta field oscillations in the hippocampus, as found in SWS. Second, HIPP theta oscillations entail bidirectional theta-rhythmic interactions between MS and HIPP.

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Excitation of rat hippocampal neurones by the stereoisomers of cis- and trans-1-amino-1,3-cyclopentane dicarboxylate

Canadian Journal of Physiology and Pharmacology ◽

10.1139/y87-347 ◽

1987 ◽

Vol 65 (11) ◽

pp. 2196-2201 ◽

Cited By ~ 10

Author(s):

K. Curry ◽

D. S. K. Magnuson ◽

H. McLennan ◽

M. J. Peet

Keyword(s):

Membrane Potential ◽

Action Potentials ◽

Burst Firing ◽

Stratum Radiatum ◽

Side Chain ◽

Intracellular Recordings ◽

Dendritic Region ◽

Cis And Trans ◽

Rhythmic Burst ◽

Slow Depolarization

Intracellular recordings were obtained from rat hippocampal neurones during the microiontophoretic ejection of the stereoisomers of cis- and trans-1-amino-1,3-cyclopentane dicarboxylate into the dendritic region (stratum radiatum) of the impaled cells. L-(+)-cis-1-Amino-1,3-cyclopentane dicarboxylate, D-(+)-trans-1-amino-1,3-cyclopentane dicarboxylate, and 1-(−)-trans-1-amino-1,3-cyclopentane dicarboxylate all evoked patterns of excitation resembling that elicited by kainate. All of these responses were unaffected by D-(−)-2-amino-5-phosphonovalerate but were antagonized at comparable currents by kynurenate. The excitation produced by D-(−)-cis-1-amino-1,3-cyclopentane dicarboxylate was similar to that evoked by N-methyl-D-aspartate. At low ejection currents a slow depolarization triggered rhythmic burst firing, each burst consisting of a depolarizing shift in membrane potential upon which were superimposed four to five action potentials. These responses were antagonized both by D-(−)-2-amino-5-phosphonovalerate and by kynurenate. The results are discussed with respect to the conformational requirements considered to be necessary for interaction at the kainate and N-methyl-D-aspartate receptors on CA1 pyramidal neurones. It is important to note that the isopropylene side chain of kainate is absent from the 1-amino-1-3-cyclopentane dicarboxylate molecule.

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