Dendritic Calcium Plateau Potentials Modulate Input–Output Properties of Juxtaglomerular Cells in the Rat Olfactory Bulb

2006 ◽  
Vol 96 (5) ◽  
pp. 2354-2363 ◽  
Author(s):  
Zhishang Zhou ◽  
Wenhui Xiong ◽  
Arjun V. Masurkar ◽  
Wei R. Chen ◽  
Gordon M. Shepherd

Understanding the intrinsic membrane properties of juxtaglomerular (JG) cells is a necessary step toward understanding the neural basis of olfactory signal processing within the glomeruli. We used patch-clamp recordings and two-photon Ca2+ imaging in rat olfactory bulb slices to analyze a long-lasting plateau potential generated in JG cells and characterize its functional input–output roles in the glomerular network. The plateau potentials were initially generated by dendritic calcium channels. Bath application of Ni2+ (250 μM to 1 mM) totally blocked the plateau potential. A local puff of Ni2+ on JG cell dendrites, but not on the soma, blocked the plateau potentials, indicating the critical contribution of dendritic Ca2+ channels. Imaging studies with two-photon microscopy showed that a dendritic Ca2+ increase was always correlated with a dendritic but not a somatic plateau potential. The dendritic Ca2+ conductance contributed to boosting the initial excitatory postsynaptic potentials (EPSPs) to produce the plateau potential that shunted and reduced the amplitudes of the following EPSPs. This enables the JG cells to act as low-pass filters to convert high-frequency inputs to low-frequency outputs. The low frequency (2.6 ± 0.8 Hz) of rhythmic plateau potentials appeared to be determined by the intrinsic membrane properties of the JG cell. These properties of the plateau potential may enable JG cells to serve as pacemaker neurons in the synchronization and oscillation of the glomerular network.

2001 ◽  
Vol 86 (4) ◽  
pp. 1816-1825 ◽  
Author(s):  
Takeshi Otsuka ◽  
Fujio Murakami ◽  
Wen-Jie Song

The subthalamic nucleus (STN) directly innervates the output structures of the basal ganglia, playing a key role in basal ganglia function. It is therefore important to understand the regulatory mechanisms for the activity of STN neurons. In the present study, we aimed to investigate how the intrinsic membrane properties of STN neurons interact with their synaptic inputs, focusing on their generation and the properties of the long-lasting, plateau potential. Whole cell recordings were obtained from STN neurons in slices prepared from postnatal day 14 (P14) to P20 rats. We found that activation of glutamate receptor-mediated excitatory synaptic potentials (EPSPs) evoked a plateau potential in a subpopulation of STN neurons ( n = 13/22), in a voltage-dependent manner. Plateau potentials could be induced only when the cell was hyperpolarized to more negative than about −75 mV. Plateau potentials, evoked with a depolarizing current pulse, again only from a hyperpolarized state, were observed in about half of STN neurons tested ( n = 162/327). Only in neurons in which a plateau potential could be evoked by current injection did EPSPs evoke plateau potentials. L-type Ca2+ channels, Ca2+-dependent K+ channels, and TEA-sensitive K+ channels were found to be involved in the generation of the potential. The stability of the plateau potential, tested by the injection of a negative pulse current during the plateau phase, was found to be robust at the early phase of the potential, but decreased toward the end. As a result the early part of the plateau potential was resistant to membrane potential perturbations and would be able to support a train of action potentials. We conclude that excitatory postsynaptic potentials, evoked in a subpopulation of STN neurons at a hyperpolarized state, activate L-type Ca2+ and other channels, leading to the generation of a plateau potential. Thus about half of STN neurons can transform short-lasting synaptic excitation into a long train of output spikes by voltage-dependent generation of a plateau potential.


1993 ◽  
Vol 176 (1) ◽  
pp. 307-310
Author(s):  
J. C. Hancox ◽  
R. M. Pitman

Cyclical patterns of behaviour such as respiration and locomotion are generated by groups of neurones whose output depends not only upon their synaptic interconnections but also on the intrinsic membrane properties of individual cells. For example, the ionic conductances of some neurones in rhythm-generating circuits allow these cells to respond to non-patterned excitatory synaptic drive with ‘plateau’ or ‘driver’ potentials: prolonged, regenerative depolarizations which can drive bursts of impulses and, thereby, contribute to characteristics of the motor rhythm (Russell and Hartline, 1978, 1982; Tazaki and Cooke, 1979a-c, 1983a-c, 1986, 1990). Plateau potentials are not restricted to interneurones of the central pattern generator; they may also be recorded from motoneurones, which form the final output to muscles. Thus, plateau potentials have been recorded from locomotor motoneurones from the crayfish (Sillar and Elson, 1986), lamprey (Wallen and Grillner, 1987), cat (Hounsgaard et al. 1988) and turtle (Hounsgaard and Kiehn, 1989) (see also review by Kiehn, 1991).


2007 ◽  
Vol 97 (3) ◽  
pp. 1959-1968 ◽  
Author(s):  
Ramani Balu ◽  
Ben W. Strowbridge

The olfactory bulb, a second-order sensory brain region, relays afferent input from olfactory receptor neurons to piriform cortex and other higher brain centers. Although large inhibitory postsynaptic potentials (IPSPs) are evident in in vivo intracellular recordings from mitral cells, the functional significance of these synaptic responses has not been defined. In many brain regions, IPSPs can function to either inhibit spiking by transiently suppressing activity or can evoke spiking directly by triggering rebound discharges. We used whole cell patch-clamp recordings from mitral cells in olfactory bulb slices to investigate the mechanisms by which IPSPs regulate mitral cell spike discharges. Mitral cells have unusual intrinsic membrane properties that support rebound spike generation in response to small-amplitude (3–5 mV) but not large-amplitude hyperpolarizing current injections or IPSPs. Rebound spiking occurring in mitral cells was dependent on recovery of subthreshold Na currents, and could be blocked by tetrodotoxin (TTX, 1 μM) or the subthreshold Na channel blocker riluzole (10 μM). Surprisingly, larger-amplitude hyperpolarizing stimuli impeded spike generation by recruiting a transient outward IA-like current that was sensitive to high concentrations of 4-aminopyridine and Ba. The interplay of voltage-gated subthreshold Na channels and transient outward current produces a narrow range of IPSP amplitudes that generates rebound spikes. We also found that subthreshold Na channels boost subthreshold excitatory stimuli to produce membrane voltages where granule-cell-mediated IPSPs can produce rebound spikes. These results demonstrate how the intrinsic membrane properties of mitral cells enable inhibitory inputs to bidirectionally control spike output from the olfactory bulb.


Author(s):  
Ümit Suat Mayadali ◽  
Jérome Fleuriet ◽  
Michael Mustari ◽  
Hans Straka ◽  
Anja Kerstin Ellen Horn

AbstractExtraocular motoneurons initiate dynamically different eye movements, including saccades, smooth pursuit and vestibulo-ocular reflexes. These motoneurons subdivide into two main types based on the structure of the neuro-muscular interface: motoneurons of singly-innervated (SIF), and motoneurons of multiply-innervated muscle fibers (MIF). SIF motoneurons are thought to provoke strong and brief/fast muscle contractions, whereas MIF motoneurons initiate prolonged, slow contractions. While relevant for adequate functionality, transmitter and ion channel profiles associated with the morpho-physiological differences between these motoneuron types, have not been elucidated so far. This prompted us to investigate the expression of voltage-gated potassium, sodium and calcium ion channels (Kv1.1, Kv3.1b, Nav1.6, Cav3.1–3.3, KCC2), the transmitter profiles of their presynaptic terminals (vGlut1 and 2, GlyT2 and GAD) and transmitter receptors (GluR2/3, NMDAR1, GlyR1α) using immunohistochemical analyses of abducens and trochlear motoneurons and of abducens internuclear neurons (INTs) in macaque monkeys. The main findings were: (1) MIF and SIF motoneurons express unique voltage-gated ion channel profiles, respectively, likely accounting for differences in intrinsic membrane properties. (2) Presynaptic glutamatergic synapses utilize vGlut2, but not vGlut1. (3) Trochlear motoneurons receive GABAergic inputs, abducens neurons receive both GABAergic and glycinergic inputs. (4) Synaptic densities differ between MIF and SIF motoneurons, with MIF motoneurons receiving fewer terminals. (5) Glutamatergic receptor subtypes differ between MIF and SIF motoneurons. While NMDAR1 is intensely expressed in INTs, MIF motoneurons lack this receptor subtype entirely. The obtained cell-type-specific transmitter and conductance profiles illuminate the structural substrates responsible for differential contributions of neurons in the abducens and trochlear nuclei to eye movements.


1982 ◽  
Vol 48 (4) ◽  
pp. 914-937 ◽  
Author(s):  
D. F. Russell ◽  
D. K. Hartline

1. Neurons in the central pattern generator for the "pyloric" motor rhythm of the lobster stomatogastric ganglion were investigated for the possible involvement of regenerative membrane properties in their membrane-potential oscillations and bursting output patterns. 2. Evidence was found that each class of pyloric-system neurons can possess a capability for generating prolonged regenerative depolarizations by a voltage-dependent membrane mechanism. Such responses have been termed plateau potentials. 3. Several tests were applied to determine whether a given cell possessed a plateau capability. First among these was the ability to trigger all-or-none bursts of nerve impulses by brief depolarizing current pulses and to terminate bursts in an all-or-none fashion with brief hyperpolarizing current pulses. Tests were made under conditions of a high level of activity in the pyloric generator, often in conjunction with the use of hyperpolarizing offsets to the cell under test to suppress ongoing bursting. 4. For each class, the network of synaptic interconnections among the pyloric-system neurons was shown to not be the cause of the regenerative responses observed. 5. Plateau potentials are viewed as a driving force for axon spiking during bursts and as interacting with the synaptic network in the formation of the pyloric motor pattern.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Feng Yi ◽  
Tavita Garrett ◽  
Karl Deisseroth ◽  
Heikki Haario ◽  
Emily Stone ◽  
...  

AbstractParvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca ($$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB ) are essential for hippocampal rhythms and learning operations yet are poorly understood at cellular and synaptic levels. We combined electrophysiological, optogenetic, and modeling approaches to investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neuronal properties. $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neurons had intrinsic membrane properties distinct from acetylcholine- and somatostatin-containing MS-DBB subtypes. Viral expression of the fast-kinetic channelrhodopsin ChETA-YFP elicited action potentials to brief (1–2 ms) 470 nm light pulses. To investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB transmission, light pulses at 5–50 Hz frequencies generated trains of inhibitory postsynaptic currents (IPSCs) in CA1 stratum oriens interneurons. Using a similar approach, optogenetic activation of local hippocampal PV ($$\hbox {PV}_{\text{HC}}$$ PV HC ) neurons generated trains of $$\hbox {PV}_{\text{HC}}$$ PV HC -mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to $$\hbox {PV}_{\text{HC}}$$ PV HC synapses, $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses possessed lower initial release probability, transiently resisted STD at gamma (20–50 Hz) frequencies, and recovered more rapidly from synaptic depression. Experimentally-constrained mathematical synapse models explored mechanistic differences. Relative to the $$\hbox {PV}_{\text{HC}}$$ PV HC model, the $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.


1998 ◽  
Vol 15 (2) ◽  
pp. 217-221 ◽  
Author(s):  
Michelle C. Storey ◽  
J. G. Greenhill ◽  
T. Kotani

AbstractObservational and theoretical evidence points to the existence of an unusually high magnetic field on GX 1+4. The pulsar is thus an ideal laboratory for studying two-photon cyclotron emission, an important source of photons of frequency significantly less than the cyclotron frequency in X-ray pulsars. Low-frequency approximations to the two-photon cyclotron emission transition probabilities are derived. These are used to calculate the theoretical opening angle of the double-humped pulse shape predicted by the two-photon cyclotron emission model. The theoretical pulse shape, incorporating the effects of gravitational light bending, is compared with observations of GX 1+4. Observed light curves have opening angles consistent with the theoretically predicted maximum value.


2005 ◽  
Vol 94 (5) ◽  
pp. 3357-3367 ◽  
Author(s):  
Elodie Christophe ◽  
Nathalie Doerflinger ◽  
Daniel J. Lavery ◽  
Zoltán Molnár ◽  
Serge Charpak ◽  
...  

Previous studies have shown that layer V pyramidal neurons projecting either to subcortical structures or the contralateral cortex undergo different morphological and electrophysiological patterns of development during the first three postnatal weeks. To isolate the determinants of this differential maturation, we analyzed the gene expression and intrinsic membrane properties of layer V pyramidal neurons projecting either to the superior colliculus (SC cells) or the contralateral cortex (CC cells) by combining whole cell recordings and single-cell RT-PCR in acute slices prepared from postnatal day (P) 5–7 or P21–30 old mice. Among the 24 genes tested, the calcium channel subunits α1B and α1C, the protease Nexin 1, and the calcium-binding protein calbindin were differentially expressed in adult SC and CC cells and the potassium channel subunit Kv4.3 was expressed preferentially in CC cells at both stages of development. Intrinsic membrane properties, including input resistance, amplitude of the hyperpolarization-activated current, and action potential threshold, differed quantitatively between the two populations as early as from the first postnatal week and persisted throughout adulthood. However, the two cell types had similar regular action potential firing behaviors at all developmental stages. Surprisingly, when we increased the duration of anesthesia with ketamine–xylazine or pentobarbital before decapitation, a proportion of mature SC cells, but not CC cells, fired bursts of action potentials. Together these results indicate that the two populations of layer V pyramidal neurons already start to differ during the first postnatal week and exhibit different firing capabilities after anesthesia.


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