Subthreshold membrane potential oscillations

Last updated
Figure 1. Illustration for Subthreshold Membrane Potential Oscillations.jpg
Figure 1.

Subthreshold membrane potential oscillations are membrane oscillations that do not directly trigger an action potential since they do not reach the necessary threshold for firing. However, they may facilitate sensory signal processing.

Contents

Neurons produce action potentials when their membrane potential increases past a critical threshold. In order for neurons to reach threshold for action potential to fire, enough sodium (Na+) ions must enter the cell through voltage gated sodium channels through membrane and depolarize the cell. [1] The threshold is reached to overcome the electrochemical equilibrium within a neuron, where there is a balance between potassium ions (K+) moving down their concentration gradient (inside the cell to outside), and the electrical gradient that prevents K+ from moving down its own gradient. [2] Once the threshold value is reached, an action potential is produced, causing a rapid increase of Na+ enters the cell with more Na+ channels along the membrane opening, resulting in a rapid depolarization of the cell. [1] Once the cell has been depolarized, voltage-gated sodium channels close, causing potassium channels to open; K+ ions then proceed to move against their concentration gradient out of the cell. [3]

However, if the voltage is below the threshold, the neuron does not fire, but the membrane potential still fluctuates due to postsynaptic potentials and intrinsic electrical properties of neurons. Therefore, these subthreshold membrane potential oscillations do not trigger action potentials, since the firing of an action potential is an "all-or-nothing" response, and these oscillations do not allow for the depolarization of the neuron to reach the threshold needed, which is typically around -55 mV; [4] an "all-or-nothing" response refers to the ability of a neuron to fire an action potential only after reaching the exact threshold. [3] For example, figure 1 depicts the localized nature and the graded potential nature of these subthreshold membrane potential oscillations, also giving a visual representation of their placement on an action potential graph, comparing subthreshold oscillations versus a fire above the threshold. In some types of neurons, the membrane potential can oscillate at specific frequencies. These oscillations can produce firing by joining with depolarizations. [5] Although subthreshold oscillations do not directly result in neuronal firing, they may facilitate synchronous activity of neighboring neurons. It may also facilitate computation, particularly processing of sensory signals. [5] All in all, although the subthreshold membrane potential oscillations do not produce action potentials by themselves, through summation, they are able to still impact action potential outcomes.

Overview

Neurons display, beyond synaptic and action potentials, rhythmic subthreshold membrane potential oscillations (a particular type of neural oscillations). These oscillations, which resembled sinusoidal wave forms, were originally discovered in the mammalian inferior olive nucleus cells. [6] The functional relevance of subthreshold oscillations concerns the nature of the intrinsic electrical properties of neurons; that is, the electrical responsiveness are not derived from interactions with other cells. These properties define the dynamic phenotype independently from form or connectivity. Subthreshold oscillation frequency can vary, from few Hz to over 40 Hz, and their dynamic properties have been studied in detail in relation to neuronal activity coherence and timing in CNS, in particular with respect to the 10 Hz physiological tremor that controls motor execution, Theta rhythm in the entorhinal cortex, [7] and gamma band activity in cortical inhibitory interneurons [8] and in thalamus neurons. [9] They have also been described and studied in layers V of the entorhinal cortex, [10] [11] [12] the inferior olive in vivo, [13] the olfactory bulb [14] and the dorsal cochlear nucleus. [15] These neurons have been a major input into the cerebellum, as well, and have been found to contribute to the overall generation of movement patterns. [5] The dynamic aspects of such oscillations have been defined using mathematical modeling. [16] [17]

Based on the analysis done by Bohemer et al., the hypothalamic supraoptic nucleus (SON) contains two major populations of magnocellular neurosecretory neurons which produces and secretes vasopressin and oxytocin, respectively. [18] The study examined electrophysiological properties and ionic bases of subthreshold oscillation of the membrane potential in 104 magnocellular neurons of rats, using intracellular recording techniques. The study found that SMOP that occurred in all neurons examined were voltage-dependent; oscillation was not a result of excitatory or inhibitory activity and neither was it from an electric coupling. [18] This suggests that the subthreshold oscillation of the membrane potential may be crucial for inter-neuronal synchronization of discharge and for the amplification of synaptic events. [18]

Neurons of a subpopulation of supraoptic neurosecretory cells are able to generate phasic bursts of action potentials. In the neurons examined in this experiment, action potentials are succeeded by a depolarizing after-potential. [18] Another article investigated the effect of GABAergic input, an example of an inhibitor, to the model of the fast-spiking neuron. They suggested that inhibitory input will be able to induce a stuttering episode in these cells. [19] [20] [21]

GABA, an important neurotransmitter, is involved with modulating synaptic firing within the brain. It's been found that inhibitory neurons, including GABA, depolarize synchronously with excitatory neurons. However, they exhibit varying activities during different brain states. [22] This inhibitor is critical for sustaining subthreshold membrane potential oscillations and for excitatory synaptic impulses. Maintaining the equilibrium of GABA presence in the synapse (release and reuptake of GABA) is necessary for these rhythmic subthreshold membrane potential oscillations to occur. [23] [24]

In addition to neurons firing action potentials, they can also perform synchronized spiking or bursts. Subthreshold membrane potential oscillations do not create an action potential; however, neurons do experience bursting when they group together and create a synchronized potential by firing all at once, which is usually the result of these subthreshold potentials. [25]

Several studies have used various techniques to study the frequency of subthreshold oscillations at a different membrane potential. For example, a study examined the frequencies of SMPO in different anatomical positions on the dorsoventral axis of a rat medial entorhinal cortex. [19] They used whole-cell patch recording in vivo and biophysical modeling in compartmental simulations of entorhinal stellate cells to examine the properties (SMPO), at different membrane potentials of the entorhinal cortex layer II stellate cells. [19] [7] [8] This technique incorporates electrical stimulation of polar molecules in cell membrane. [26] The study found that Dorsal cells are likely to show a positive slope of peak frequency with depolarization, whereas ventral cells tend to show a negative slope of peak frequency with depolarization. These findings illustrate that there are high frequencies of SMPO in dorsal cells and low frequencies in the ventral cells. [13] [19] A similar study that did whole-cell recordings of olivary neurons in vivo to investigate the relationship between subthreshold activities and spiking behavior in an intact brain illustrates that the majority of neurons displayed subthreshold oscillation activities. [6] Which means that the inferior olive of mammals’ brain exhibits relatively stable frequencies settings of oscillations. [18] [6] As a result, this might be used to generate and rest temporal firing patterns in an electrically coupled ensemble. [6] [19]

Sensory Circuits

Subthreshold membrane potential oscillations play an important role in the development of the sensory systems, including, but not being limited to the visual system and the olfactory system.

In the visual system, through the help of electroencephalogram or EEG readings, the subthreshold membrane potential oscillations help equip the cortex for not only processing visual stimulation, but also neuronal plasticity. [2] These oscillations are present even before birth and also before a newborn opens its eyes, as they are forms of maturation and preparation of the human sensory cortex, which is a part of the cerebral cortex that is responsible for processing and encoding sensory information. [2] This subthreshold activity is responsible for shaping circuits for maturation and are especially distinct in the retina, in the form of retinal waves. [2]

In the olfactory system, responsible for sense of smell, according to the study, subthreshold membrane potential oscillations present in mitral cells, which are neurons in the olfactory system, are said to influence the timing of the spikes of action potentials, which in turn allows for the synchronization of multiple mitral cells. [27] The study also mentions how this oscillatory activity is thought to also impact excitatory postsynaptic potentials in the way that they act as refinement tools to this post neural activity. [27]

See also

Related Research Articles

<span class="mw-page-title-main">Chemical synapse</span> Biological junctions through which neurons signals can be sent

Chemical synapses are biological junctions through which neurons' signals can be sent to each other and to non-neuronal cells such as those in muscles or glands. Chemical synapses allow neurons to form circuits within the central nervous system. They are crucial to the biological computations that underlie perception and thought. They allow the nervous system to connect to and control other systems of the body.

<span class="mw-page-title-main">Action potential</span> Neuron communication by electric impulses

An action potential occurs when the membrane potential of a specific cell rapidly rises and falls. This depolarization then causes adjacent locations to similarly depolarize. Action potentials occur in several types of animal cells, called excitable cells, which include neurons, muscle cells, and in some plant cells. Certain endocrine cells such as pancreatic beta cells, and certain cells of the anterior pituitary gland are also excitable cells.

An inhibitory postsynaptic potential (IPSP) is a kind of synaptic potential that makes a postsynaptic neuron less likely to generate an action potential. IPSPs were first investigated in motorneurons by David P. C. Lloyd, John Eccles and Rodolfo Llinás in the 1950s and 1960s. The opposite of an inhibitory postsynaptic potential is an excitatory postsynaptic potential (EPSP), which is a synaptic potential that makes a postsynaptic neuron more likely to generate an action potential. IPSPs can take place at all chemical synapses, which use the secretion of neurotransmitters to create cell to cell signalling. Inhibitory presynaptic neurons release neurotransmitters that then bind to the postsynaptic receptors; this induces a change in the permeability of the postsynaptic neuronal membrane to particular ions. An electric current that changes the postsynaptic membrane potential to create a more negative postsynaptic potential is generated, i.e. the postsynaptic membrane potential becomes more negative than the resting membrane potential, and this is called hyperpolarisation. To generate an action potential, the postsynaptic membrane must depolarize—the membrane potential must reach a voltage threshold more positive than the resting membrane potential. Therefore, hyperpolarisation of the postsynaptic membrane makes it less likely for depolarisation to sufficiently occur to generate an action potential in the postsynaptic neurone.

<span class="mw-page-title-main">Stimulus (physiology)</span> Detectable change in the internal or external surroundings

In physiology, a stimulus is a detectable change in the physical or chemical structure of an organism's internal or external environment. The ability of an organism or organ to detect external stimuli, so that an appropriate reaction can be made, is called sensitivity (excitability). Sensory receptors can receive information from outside the body, as in touch receptors found in the skin or light receptors in the eye, as well as from inside the body, as in chemoreceptors and mechanoreceptors. When a stimulus is detected by a sensory receptor, it can elicit a reflex via stimulus transduction. An internal stimulus is often the first component of a homeostatic control system. External stimuli are capable of producing systemic responses throughout the body, as in the fight-or-flight response. In order for a stimulus to be detected with high probability, its level of strength must exceed the absolute threshold; if a signal does reach threshold, the information is transmitted to the central nervous system (CNS), where it is integrated and a decision on how to react is made. Although stimuli commonly cause the body to respond, it is the CNS that finally determines whether a signal causes a reaction or not.

<span class="mw-page-title-main">Threshold potential</span> Critical potential value

In electrophysiology, the threshold potential is the critical level to which a membrane potential must be depolarized to initiate an action potential. In neuroscience, threshold potentials are necessary to regulate and propagate signaling in both the central nervous system (CNS) and the peripheral nervous system (PNS).

Postsynaptic potentials are changes in the membrane potential of the postsynaptic terminal of a chemical synapse. Postsynaptic potentials are graded potentials, and should not be confused with action potentials although their function is to initiate or inhibit action potentials. They are caused by the presynaptic neuron releasing neurotransmitters from the terminal bouton at the end of an axon into the synaptic cleft. The neurotransmitters bind to receptors on the postsynaptic terminal, which may be a neuron or a muscle cell in the case of a neuromuscular junction. These are collectively referred to as postsynaptic receptors, since they are on the membrane of the postsynaptic cell.

An apical dendrite is a dendrite that emerges from the apex of a pyramidal cell. Apical dendrites are one of two primary categories of dendrites, and they distinguish the pyramidal cells from spiny stellate cells in the cortices. Pyramidal cells are found in the prefrontal cortex, the hippocampus, the entorhinal cortex, the olfactory cortex, and other areas. Dendrite arbors formed by apical dendrites are the means by which synaptic inputs into a cell are integrated. The apical dendrites in these regions contribute significantly to memory, learning, and sensory associations by modulating the excitatory and inhibitory signals received by the pyramidal cells.

<span class="mw-page-title-main">Neural oscillation</span> Brainwaves, repetitive patterns of neural activity in the central nervous system

Neural oscillations, or brainwaves, are rhythmic or repetitive patterns of neural activity in the central nervous system. Neural tissue can generate oscillatory activity in many ways, driven either by mechanisms within individual neurons or by interactions between neurons. In individual neurons, oscillations can appear either as oscillations in membrane potential or as rhythmic patterns of action potentials, which then produce oscillatory activation of post-synaptic neurons. At the level of neural ensembles, synchronized activity of large numbers of neurons can give rise to macroscopic oscillations, which can be observed in an electroencephalogram. Oscillatory activity in groups of neurons generally arises from feedback connections between the neurons that result in the synchronization of their firing patterns. The interaction between neurons can give rise to oscillations at a different frequency than the firing frequency of individual neurons. A well-known example of macroscopic neural oscillations is alpha activity.

Theta waves generate the theta rhythm, a neural oscillation in the brain that underlies various aspects of cognition and behavior, including learning, memory, and spatial navigation in many animals. It can be recorded using various electrophysiological methods, such as electroencephalogram (EEG), recorded either from inside the brain or from electrodes attached to the scalp.

<span class="mw-page-title-main">Mitral cell</span> Neurons that are part of the olfactory system

Mitral cells are neurons that are part of the olfactory system. They are located in the olfactory bulb in the mammalian central nervous system. They receive information from the axons of olfactory receptor neurons, forming synapses in neuropils called glomeruli. Axons of the mitral cells transfer information to a number of areas in the brain, including the piriform cortex, entorhinal cortex, and amygdala. Mitral cells receive excitatory input from olfactory sensory neurons and external tufted cells on their primary dendrites, whereas inhibitory input arises either from granule cells onto their lateral dendrites and soma or from periglomerular cells onto their dendritic tuft. Mitral cells together with tufted cells form an obligatory relay for all olfactory information entering from the olfactory nerve. Mitral cell output is not a passive reflection of their input from the olfactory nerve. In mice, each mitral cell sends a single primary dendrite into a glomerulus receiving input from a population of olfactory sensory neurons expressing identical olfactory receptor proteins, yet the odor responsiveness of the 20-40 mitral cells connected to a single glomerulus is not identical to the tuning curve of the input cells, and also differs between sister mitral cells. Odorant response properties of individual neurons in an olfactory glomerular module. The exact type of processing that mitral cells perform with their inputs is still a matter of controversy. One prominent hypothesis is that mitral cells encode the strength of an olfactory input into their firing phases relative to the sniff cycle. A second hypothesis is that the olfactory bulb network acts as a dynamical system that decorrelates to differentiate between representations of highly similar odorants over time. Support for the second hypothesis comes primarily from research in zebrafish.

<span class="mw-page-title-main">Grid cell</span>

A grid cell is a type of neuron within the entorhinal cortex that fires at regular intervals as an animal navigates an open area, allowing it to understand its position in space by storing and integrating information about location, distance, and direction. Grid cells have been found in many animals, including rats, mice, bats, monkeys, and humans.

<span class="mw-page-title-main">Synaptic gating</span>

Synaptic gating is the ability of neural circuits to gate inputs by either suppressing or facilitating specific synaptic activity. Selective inhibition of certain synapses has been studied thoroughly, and recent studies have supported the existence of permissively gated synaptic transmission. In general, synaptic gating involves a mechanism of central control over neuronal output. It includes a sort of gatekeeper neuron, which has the ability to influence transmission of information to selected targets independently of the parts of the synapse upon which it exerts its action.

Plateau potentials, caused by persistent inward currents (PICs), are a type of electrical behavior seen in neurons.

<span class="mw-page-title-main">Afterhyperpolarization</span>

Afterhyperpolarization, or AHP, is the hyperpolarizing phase of a neuron's action potential where the cell's membrane potential falls below the normal resting potential. This is also commonly referred to as an action potential's undershoot phase. AHPs have been segregated into "fast", "medium", and "slow" components that appear to have distinct ionic mechanisms and durations. While fast and medium AHPs can be generated by single action potentials, slow AHPs generally develop only during trains of multiple action potentials.

Recurrent thalamo-cortical resonance is an observed phenomenon of oscillatory neural activity between the thalamus and various cortical regions of the brain. It is proposed by Rodolfo Llinas and others as a theory for the integration of sensory information into the whole of perception in the brain. Thalamocortical oscillation is proposed to be a mechanism of synchronization between different cortical regions of the brain, a process known as temporal binding. This is possible through the existence of thalamocortical networks, groupings of thalamic and cortical cells that exhibit oscillatory properties.

Low-threshold spikes (LTS) refer to membrane depolarizations by the T-type calcium channel. LTS occur at low, negative, membrane depolarizations. They often follow a membrane hyperpolarization, which can be the result of decreased excitability or increased inhibition. LTS result in the neuron reaching the threshold for an action potential. LTS is a large depolarization due to an increase in Ca2+ conductance, so LTS is mediated by calcium (Ca2+) conductance. The spike is typically crowned by a burst of two to seven action potentials, which is known as a low-threshold burst. LTS are voltage dependent and are inactivated if the cell's resting membrane potential is more depolarized than −60mV. LTS are deinactivated, or recover from inactivation, if the cell is hyperpolarized and can be activated by depolarizing inputs, such as excitatory postsynaptic potentials (EPSP). LTS were discovered by Rodolfo Llinás and coworkers in the 1980s.

Synaptic noise refers to the constant bombardment of synaptic activity in neurons. This occurs in the background of a cell when potentials are produced without the nerve stimulation of an action potential, and are due to the inherently random nature of synapses. These random potentials have similar time courses as excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs), yet they lead to variable neuronal responses. The variability is due to differences in the discharge times of action potentials.

<span class="mw-page-title-main">Nonsynaptic plasticity</span> Form of neuroplasticity

Nonsynaptic plasticity is a form of neuroplasticity that involves modification of ion channel function in the axon, dendrites, and cell body that results in specific changes in the integration of excitatory postsynaptic potentials and inhibitory postsynaptic potentials. Nonsynaptic plasticity is a modification of the intrinsic excitability of the neuron. It interacts with synaptic plasticity, but it is considered a separate entity from synaptic plasticity. Intrinsic modification of the electrical properties of neurons plays a role in many aspects of plasticity from homeostatic plasticity to learning and memory itself. Nonsynaptic plasticity affects synaptic integration, subthreshold propagation, spike generation, and other fundamental mechanisms of neurons at the cellular level. These individual neuronal alterations can result in changes in higher brain function, especially learning and memory. However, as an emerging field in neuroscience, much of the knowledge about nonsynaptic plasticity is uncertain and still requires further investigation to better define its role in brain function and behavior.

Sharp waves and ripples (SWRs) are oscillatory patterns produced by extremely synchronised activity of neurons in the mammalian hippocampus and neighbouring regions which occur spontaneously in idle waking states or during NREM sleep. They can be observed with a variety of imaging methods, such as EEG. They are composed of large amplitude sharp waves in local field potential and produced by tens of thousands of neurons firing together within 30–100 ms window. They are some of the most synchronous oscillations patterns in the brain, making them susceptible to pathological patterns such as epilepsy.They have been extensively characterised and described by György Buzsáki and have been shown to be involved in memory consolidation in NREM sleep and the replay of memories acquired during wakefulness.

Lisa Giocomo is an American neuroscientist who is a Professor in the Department of Neurobiology at Stanford University School of Medicine. Giocomo probes the molecular and cellular mechanisms underlying cortical neural circuits involved in spatial navigation and memory.

References

  1. 1 2 Barnett, Mark W.; Larkman, Philip M. (2007-06-01). "The action potential". Practical Neurology. 7 (3): 192–197. ISSN   1474-7758. PMID   17515599.
  2. 1 2 3 4 Neuroscience. Purves, Dale, 1938- (5th ed.). Sunderland, Mass.: Sinauer Associates. 2012. ISBN   9780878936953. OCLC   754389847.{{cite book}}: CS1 maint: others (link)
  3. 1 2 Hopfield, J. J. (6 July 1995). "Pattern recognition computation using action potential timing for stimulus representation". Nature. 376 (6535): 33–36. Bibcode:1995Natur.376...33H. doi:10.1038/376033a0. ISSN   0028-0836. PMID   7596429. S2CID   4324368.
  4. ↑ Bean, Bruce P. (2007). "The action potential in mammalian central neurons". Nature Reviews Neuroscience. 8 (6): 451–465. doi:10.1038/nrn2148. PMID   17514198. S2CID   205503852.
  5. 1 2 3 Lampl, I.; Yarom, Y. (1993-11-01). "Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device". Journal of Neurophysiology. 70 (5): 2181–2186. doi:10.1152/jn.1993.70.5.2181. ISSN   0022-3077. PMID   8294979.
  6. 1 2 3 4 Lampl, Ilan (November 1993). "Subthreshold Oscillations of the Membrane Potential: A Functional Synchronizing and Timing Device" (PDF). Journal of Neurophysiology. 70 (5): 2181–6. doi:10.1152/jn.1993.70.5.2181. PMID   8294979. S2CID   18130003. Archived from the original (PDF) on 2019-02-18.
  7. 1 2 Alonso, A. <<gwmw class="ginger-module-highlighter-mistake-type-1" id="gwmw-15727248305061922973702">gwmw</gwmw> class="ginger-module-highlighter-mistake-<gwmw class="ginger-module-highlighter-mistake-type-1" id="gwmw-15727248305065175080895">anim</gwmw> ginger-module-highlighter-mistake-type-1" id="<gwmw class="ginger-module-highlighter-mistake-type-1" id="gwmw-15727248305063880507750">gwmw</gwmw>-15693837406294585512759">and</<gwmw class="ginger-module-highlighter-mistake-type-1" id="gwmw-15727248305067576128425">gwmw</gwmw>> Llinas, R. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837406397709199716">(</gwmw>1989) "Subthreshold Na+-dependent theta-like <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837406398142511287">rhythmicity</gwmw> in entorhinal cortex layer II stellate cells". Nature, 342: 175-177., gamma band in cortical inhibitory interneurons
  8. 1 2 Llinas R. Grace, A.A. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837406798165487204">and</gwmw> Yarom, Y. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837406892093294498">(</gwmw>1991) " In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10 to 50 Hz frequency range". PNAS, 88, 897-901
  9. ↑ Pedroarena, C. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837407215525912712">and</gwmw> Llinas, R. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837407318939579786">(</gwmw>1997) "Dendritic calcium conductances generate <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837407317080343964">high frequency oscillation</gwmw> in thalamocortical neurons". PNAS, 94: 724-728
  10. ↑ Schmitz D.1; Gloveli T.; Behr J.; Dugladze T.and Heinemann U. (1998). “<gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837407756583858628">Subthreshold</gwmw> membrane potential oscillations in neurons of deep layers of the entorhinal cortex”. Neuroscience, 85:. 999-1004
  11. ↑ Agrawal N, Hamam BN, Magistretti J, Alonso A, Ragsdale DS. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837408208239423145">(</gwmw>1999)."Persistent sodium channel activity mediates subthreshold membrane potential oscillations and low-threshold spikes in rat entorhinal cortex layer V neurons." J. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837408545591622839">Gen</gwmw>. Physiol 114:491-509
  12. ↑ Giocomo L. M., Zilli, E A. Fransén, E, and Hasselmo M.E. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837409155534057589">(</gwmw>2007).“Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing” Science 315: 1719 - 1722
  13. 1 2 Khosrovani, S., Van Der Giessen, R. S., De Zeeuw C. I., and De Jeu M. T. G. (2007). “In <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837410219340631534">vivo</gwmw> mouse inferior olive neurons exhibit heterogeneous subthreshold oscillations and spiking patterns” PNAS 104 : 15911-15916
  14. ↑ Desmaisons, D., Vincent J.D. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837410578285721734">and</gwmw> Lledo, P.M. (1999). “Control of action potential timing <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837410855023490751">by</gwmw> intrinsic subthreshold oscillations in the olfactory bulb output neurons”. J, Neuroscience 19: 10727-10737
  15. ↑ Manis, P.B., Molitor, S.C. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837411331385507072">and</gwmw> Wu, <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837411332257506228">H.</gwmw>(1999) “Subthreshold oscillations generated by TTX-sensitive sodium currents in dorsal cochlear nucleus pyramidal cells”. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837411504100542584">Exp</gwmw>. Brain Research 153: 443-451
  16. ↑ Hutcheon, B and Yarom, Y. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837411979407237284">(</gwmw>2000) "Resonance, oscillation and the intrinsic frequency preferences of neurons" TINS 23:216-222
  17. ↑ Izhikevich E.M., Desai, N.S, Walcott, E.C. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-1" id="gwmw-15693837412309330060396">Hoppensteadt</gwmw>. <gwmw class="ginger-module-highlighter-mistake-anim ginger-module-highlighter-mistake-type-3" id="gwmw-15693837412493329772884">(</gwmw>2003) "Bursts as a unit of neural information: selective communication via resonance TINS" 26:161-167.
  18. 1 2 3 4 5 Boehmer, Gerd; Greffrath, Wolfgang; Martin, Erich; Hermann, Sven (July 2000). "Subthreshold oscillation of the membrane potential in magnocellular neurones of the rat supraoptic nucleus". The Journal of Physiology. 526 (1): 115–128. doi:10.1111/j.1469-7793.2000.t01-1-00115.x. ISSN   0022-3751. PMC   2269988 . PMID   10878105.
  19. 1 2 3 4 5 Yoshida, Motoharu; Giocomo, Lisa M.; Boardman, Ian; Hasselmo, Michael E. (2011-08-31). "Frequency of Subthreshold Oscillations at Different Membrane Potential Voltages in Neurons at Different Anatomical Positions on the Dorsoventral Axis in the Rat Medial Entorhinal Cortex". The Journal of Neuroscience. 31 (35): 12683–12694. doi:10.1523/JNEUROSCI.1654-11.2011. PMC   3177240 . PMID   21880929.
  20. ↑ Wu, Nanping; Hsiao, Chie-Fang; Chandler, Scott H. (2001-06-01). "Membrane Resonance and Subthreshold Membrane Oscillations in Mesencephalic V Neurons: Participants in Burst Generation". Journal of Neuroscience. 21 (11): 3729–3739. doi:10.1523/JNEUROSCI.21-11-03729.2001. ISSN   0270-6474. PMC   6762704 . PMID   11356860.
  21. ↑ Klaus, Andreas; Hjorth, Johannes; Hellgren-Kotaleski, Jeanette (2009-07-13). "The influence of subthreshold membrane potential oscillations and GABAergic input on firing activity in striatal fast-spiking neurons". BMC Neuroscience. 10 (S1). doi: 10.1186/1471-2202-10-s1-p244 . ISSN   1471-2202.
  22. ↑ Carandini, Matteo; Haider, Bilal (2010-03-15). "Faculty of 1000 evaluation for Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice". doi: 10.3410/f.2546956.2198054 .{{cite journal}}: Cite journal requires |journal= (help)
  23. ↑ Yousuf, Muhammad Saad; Kerr, Bradley J. (2016-01-01), Barrett, James E. (ed.), "Chapter Nine - The Role of Regulatory Transporters in Neuropathic Pain", Advances in Pharmacology, Pharmacological Mechanisms and the Modulation of Pain, Academic Press, vol. 75, pp. 245–271, doi:10.1016/bs.apha.2015.12.003, PMID   26920015 , retrieved 2019-11-01
  24. ↑ Bak, Lasse K.; Schousboe, Arne; Waagepetersen, Helle S. (2006). "The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer". Journal of Neurochemistry. 98 (3): 641–653. doi: 10.1111/j.1471-4159.2006.03913.x . ISSN   1471-4159. PMID   16787421.
  25. ↑ V-GHAFFARI B; KOUHNAVARD M; KITAJIMA T (2016). "Biophysical Properties of Subthreshold Resonance Oscillations and Subthreshold Membrane Oscillations in Neurons". Journal of Biological Systems. 24 (4): 561–575. doi:10.1142/S0218339016500285. PMC   5367638 . PMID   28356608.
  26. ↑ Fertig, Niels; Blick, Robert H.; Behrends, Jan C. (June 2002). "Whole Cell Patch Clamp Recording Performed on a Planar Glass Chip". Biophysical Journal. 82 (6): 3056–3062. Bibcode:2002BpJ....82.3056F. doi:10.1016/s0006-3495(02)75646-4. ISSN   0006-3495. PMC   1302093 . PMID   12023228.
  27. 1 2 Desmaisons, David; Vincent, Jean-Didier; Lledo, Pierre-Marie (1999-12-15). "Control of Action Potential Timing by Intrinsic Subthreshold Oscillations in Olfactory Bulb Output Neurons". The Journal of Neuroscience. 19 (24): 10727–10737. doi: 10.1523/jneurosci.19-24-10727.1999 . ISSN   0270-6474. PMC   6784925 . PMID   10594056.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.