Intrinsic plasticity

• Robert H. Cudmore, Department of Neuroscience, The Johns Hopkins University School of Medicine

• Dr. Niraj S. Desai, The University of Texas at Austin, Austin, Texas, United

Intrinsic plasticity is the persistent modification of a neuron’s intrinsic electrical properties by neuronal or synaptic activity. It is mediated by changes in the expression level or biophysical properties of ion channels in the membrane, and can affect such diverse processes as synaptic integration, subthreshold signal propagation, spike generation, spike backpropagation, and meta-plasticity. The function of intrinsic plasticity in behaving animals is uncertain but there is experimental evidence for several distinct roles: as part of the memory engram itself, as a regulator of synaptic plasticity underlying learning and memory, and as a component of homeostatic regulation.

It is important to note that intrinsic plasticity is distinct from synaptic plasticity, which involves changes at the synapse between two neurons rather than changes in the electrical properties within a single neuron. It is also important to note that there are closely-related phenomena that can affect a neuron's excitability – such as neuromodulation, structural plasticity, short-term plasticity due to channel kinetics, and neurodevelopment – but which are generally excluded from the term intrinsic plasticity.

Figure 1: (A) Schematic of the role of intrinsic excitability in synaptic integration to generate action potential output. The shape of incoming postsynaptic potentials are primarily determined by the properties of the synapses (synaptic input). These postsynaptic potentials are spatially and temporally modified by the activation of postsynaptic ion channels (postsynaptic processing). This modification of incoming synaptic input ultimately determines if and when an action potential will be generated (AP output). (B) A neurons transfer function. Neurons translate synaptic input into AP output. Changes in this transfer function will, given the same synaptic input, produce different output. This plasticity of the transfer function is mediated by the properties of postsynaptic ion channels.

Types of intrinsic plasticity

How a neuron with a given morphology integrates synaptic input to produce action potential output is determined by the number, type, and distribution of its voltage- and calcium-gated ion channels. Broadly speaking, channels in the dendrites are responsible for synaptic integration, whereas those near the soma and axon hillock are responsible for action potential generation and slow wave generation such as in rhythmic or pacemaker activity. Experiments, mainly using in vitro preparations, have shown that all of these features are plastic and can be modified by different kinds of neural activity. Again speaking broadly: 1) strong, transient synaptic or somatic stimulation tends to produce an increased ability to generate spikes, a phenomenon called long-term potentiation of intrinsic excitability (LTP-IE); 2) long-lasting stimulation (or deprivation) – and especially a prolonged modulation of background activity – tends to reduce (or increase) intrinsic excitability resulting in a form of homeostatic plasticity; and 3) synaptic stimulation localized to dendritic areas can locally modify channel numbers and properties in ways that affect the dendritic integration of synaptic inputs. All of these effects have been shown in vitro to be long lasting (hours to days). Comprehensive reviews are given by Daoudal and Debanne (2003), Zhang and Linden (2003), and Frick and Johnston (2005).

LTP-IE

• E-S potentiation: Many of the same experimental protocols used to study synaptic plasticity also give rise to intrinsic plasticity. This is true even of hippocampal long-term potentiation (LTP). After LTP induction, the probability of discharge of postsynaptic neurons in response to excitatory postsynaptic potentials (EPSPs) is increased, a phenomenon known as E-S potentiation (Bliss and Lomo, 1973). Part of this enhanced excitability is due to the altered balance between excitation and inhibition, but part is due to intrinsic changes in both postsynaptic and presynaptic neurons. In particular, the number of action potentials generated by pyramidal neurons in response to current injection increases after LTP induction and spike threshold decreases (Chavez-Noriega et al., 1990). Several different ion channels, including delayed-rectifier potassium, transient sodium, and hyperpolarization-activated, have been implicated. The effects are bidirectional: induction of long-term synaptic depression (LTD) reduces postsynaptic and presynaptic excitability (Daoudal et al., 2002; Li et al., 2004).

• Burst firing Induction of synaptic plasticity is not necessary for the induction of LTP-IE. In fact, repeated injection of depolarizing current to produce postsynaptic APs in the absence of synaptic stimulation reduces spike threshold and increases the number of spikes elicited by current in both cortical pyramidal neurons and cerebellar deep nuclei (Aizenman and Linden, 2000; Cudmore and Turrigiano, 2004). The excitability of cerebellar granule cells can likewise be increased by a weak theta-burst stimulation to the mossy fibers that fails to induce synaptic LTP (Armano et al., 2000).

• mGluR activation: In both neocortex and hippocampus, a relationship between activation of type I metabotropic glutamate receptors (mGluRs) and pyramidal neuron intrinsic excitability has been demonstrated. mGluR activation, whether by synaptic stimulation or pharmacological treatment, reduces spike frequency adaptation by suppressing medium and/or slow afterhyperpolarization (AHP) currents (Ireland and Abraham, 2002; Sourdet et al., 2003).

• Vestibular inhibition: Excitability changes can also be driven by inhibition. Neurons of the medial vestibular nucleus in the mammalian brainstem become more excitable after brief periods (minutes) inhibitory synaptic stimulation or direct hyperpolarizing currents (Nelson et al., 2003). This is driven by a reduction in fast AHP currents (BK-type).

Homeostatic plasticity of intrinsic excitability

• Crustacean STG: The crustacean stomatogastric ganglion (STG) has been an important model system for the study of intrinsic plasticity. STG neurons participate in motor programs that produce rhythmic movements; this rhythmic pattern is dependent on the ability of STG neurons to fire in bursts. When neurons are pharmacologically isolated from their natural inputs, they initially fire tonically rather than in bursts, but then over time burst firing reappears due to coordinated changes in calcium and potassium conductances that compensate for the absence of synaptic drive (Turrigiano et al., 1994; Haedo and Golowasch, 2006).

• Cortex & hippocampus: Depriving neocortical or hippocampal neurons of synaptic or electrical activity for extended periods (tens of minutes to days) has been found in several studies to result in an upregulation of intrinsic excitability, in a manner that appears to counteract the acute effects of deprivation (Desai et al., 1999; Karmarkar and Buonomano, 2006). That is, it appears to be homeostatic in action. On the other hand, boosting activity above basal levels drives excitability in the opposite direction. The ion channels modified by activity vary between cell types and brain areas; they include those responsible for sustained potassium, transient sodium, leak, and hyperpolization-activated currents (Aptowicz et al., 2004; Gibson et al., 2006; Van Welie et al., 2004, 2006).

• Xenopus: Exposing freely-swimming Xenopus tadpoles to 4-5 hours of persistent visual stimulation increases the excitability of optic tectal neurons, due to an enhancement of sodium currents (Aizenman et al., 2003). At the same time the stimulation reduces excitatory synaptic drive. Together the changes are thought to improve signal-to-noise by making the visual system less responsive to background activity but more responsive to brief, strong visual stimuli.

Plasticity of dendritic integration

• EPSP summation: Protocols that induce synaptic plasticity are accompanied not only by changes in global intrinsic excitability (i.e., the spike generating mechanism), but local changes in synaptic integration. In hippocampal CA1 neurons, stimulating neighboring but separate synaptic pathways generally results in EPSP summation that is sublinear. Inducing LTP (or LTD) at one of the pathways improves (or degrades) summation. At more distal synapses, the effect is significant only if the EPSPs arrive near synchronously (~5 ms), suggesting that intrinsic plasticity can regulate coincidence detection. These changes appear to be mediated by changes in some combination of A-type and hyperpolarization-activated conductances (Frick et al., 2004; Xu et al., 2006; Kim et al., 2007).

• AP backpropagation: While action potentials are (normally) initiated at the axon hillock and soma, the resulting deflection propagates both forward down the axon and backward into the dendrites. The backpropagating AP is thought to be an important signaling element in Hebbian synaptic plasticity, and depends on the ion channels distributed along the dendritic tree. Induction of synaptic LTP in CA1 pyramidal neurons enhances AP backpropagation and associated calcium influx (Tsubokawa et al., 2000; Frick et al., 2004). The effects are localized to the dendritic region containing the potentiated synapses and are mediated by regulation of A-type potassium channels.

Intrinsic plasticity & learning

Evidence that intrinsic plasticity accompanies, and may help mediate, learning has been obtained in both invertebrates and mammals. In most experiments (but not all), the type of learning involved was associative conditioning. Several of the best-studied examples are given here; others are given by Zhang and Linden (2003).

Invertebrates

• Hermissenda: The sea slug Hermissenda has a tendency to move towards light (phototaxis), but when light is paired with rotation, an aversive stimulus, there is an increase in the latency to approach the light. This behavior can last for weeks and is associative, as it does not result when light and rotation are presented in an uncorrelated way (Alkon et al., 1982; Alkon, 1984). Extensive intracellular experiments from neurons in intact and reduced preparations have demonstrated that this learning is mediated largely, and perhaps exclusively, by an increase in the intrinsic excitability of type B photoreceptors in the Hermissenda eye (Gandhi and Matzel, 2000). This increased excitability is caused by a downregulation of A-type and calcium-sensitive potassium currents, persists as long as the learned response, and is positively correlated with the magnitude of the response.

• Aplysia: Siphon withdrawal in the mollusk Aplysia has long been used as a model system to study conditioning. When a siphon tap (conditioned stimulus, CS) is paired with a tail shock (unconditioned stimulus, US), siphon withdrawal can be measured as a conditioned response (CR). This protocol results in synaptic potentiation between sensory and motor neurons, but it also increases the intrinsic excitability of sensory neurons (Antonov et al., 2001). The number of spikes elicited by a siphon tap or directly by current injection increases after conditioning. Certain intrinsic changes are also elicited in Aplysia after operant conditioning or sensitization (Cleary et al., 1998; Brembs et al., 2002).

• Helix: The snail Helix exhibits a learned behavior in which a shell tap is the CS, an air puff delivered to an opening through which air passes is the US, and reflexive closure of the opening is the CR. After repetitive pairing of US and CS, interneurons that drive closure show reduced spike threshold and depolarized resting potentials (Gainutdinov et al., 1998).

• Drosophila: The fruit fly Drosophila melanogaster can undergo several kinds of associative learning, including courtship conditioning and odor conditioning. Single gene mutations that reduce a number of potassium currents – including A-type and TEA-sensitive currents – produce flies in which learning and/or retention are abolished or severely impaired, indicating the importance of proper K+ channel function for conditioning (Daoudal and Debanne, 2003).

Mammals

• Cats: When an auditory click (CS) precedes a tap (US) between the eyebrows, a cat responds with both an eyeblink and a nose twitch (CR). Intracellular recordings in conscious animals indicate that acquisition of an association between CS and CR is accompanied by a persistent increase (lasting at least 28 days) in neuronal excitability in the part of cortex that projects (through intermediate neurons) to the facial musculature (Brons and Woody, 1980). The increased excitability persists even after the CR has been extinguished, a persistence which may be related to the faster acquisition of the CR if the animal is subsequently retrained on the same or a different associative conditioning task.

• Rabbits: The effects of eyelid conditioning on hippocampal neurons have been extensively examined using in vitro preparations. In this task, a tone serves as the CS, an airpuff or weak shock to the eyeball the US, and an eyeblink (or nictitating) response the CR. In some experiments, a trace interval is imposed between the offset of the tone and the onset of the puff or shock. After an animal acquires the CR, recordings made from subsequently-prepared hippocampal slices indicate that a substantial fraction (~50 %) of CA1 and CA3 pyramidal are more excitable (Disterhoft et al., 1986; Disterhoft et al., 1988). This excitability increase is manifested by an increased number of spikes elicited by current injection and a decreased AHP. The excitability increase is produced by a reduction in calcium-activated potassium conductances. It can last for several days following CR acquisition, but generally decays away long before the memory of the conditioning does.

• Rats (operant conditioning): Rats can be trained to discriminate odors in order to receive a reward, a form of operant conditioning. Afterwards, pyramidal neurons in the superficial layers of olfactory cortex are more intrinsically excitable (Saar et al., 1998). As in the case of eyelid conditioning, a reduction in AHP currents is thought to be responsible. The increased excitability is temporary, with membrane properties decaying back to baseline within 7 days.

• Rats (associative conditioning): The lateral amygdala is crucial for Pavlovian fear conditioning. Even in anesthetized animals, pairing an odor (CS) with a footshock (US) can result in an increased amygdalar response to the CS. In vivo intracellular recordings have revealed that this increased response is due not only to increases in synaptic strength but also in intrinsic neural excitability (Rosenkranz and Grace, 2002).

• Rats (spatial learning): The watermaze task, in which rats swimming in a tank of water attempt to locate a hidden platform, is a classic test of spatial learning. CA1 pyramidal neurons in the dorsal hippocampus of animals that learn the task are more intrinsically excitable afterwards (Oh et al., 2003). As in other forms of learning, a reduction in AHP currents is responsible.

Functions of intrinsic plasticity

The role of intrinsic plasticity in the normal functioning of nervous systems remains speculative but several possibilities exist, with varying levels of experimental and theoretical justification.

Memory engram

That memories are formed and maintained by physical alterations in the neurons that make up the circuits of the brain is undisputed. But quite what those alterations are is uncertain. Most research work on neural plasticity has focused on synaptic plasticity – on how the connections between neurons are modified by experience and learning – a focus justified by experimental evidence of synaptic LTP & LTD at numerous types of synapses, by some experimental work linking synaptic plasticity and learning, and by theoretical models that demonstrate the utility and computational power of synapse-specific plasticity. Plastic changes in intrinsic membrane properties are thought to be less important for memory encoding because the lack of temporal and spatial specificity observed in synaptic plasticity limits the computational power they impart neural circuits (even allowing for localized changes in dendritic excitability) and because, in some experiments as noted above, the time course of intrinsic plasticity is different than that of learning and memory. Nevertheless, in simple systems, as in the Hermissenda eye, experience-dependent changes in intrinsic excitability may in fact form the memory engram itself.

Meta-plasticity

In more complex systems, it seems likely that intrinsic plasticity plays an auxiliary role to synaptic plasticity in learning. In particular, by modulating spike generation mechanisms and AP backpropagation, intrinsic plasticity may act as gate or a regulator of the synaptic changes that physically underlie learning, sometimes making synaptic plasticity more likely, sometimes less likely. This seems plausible given the importance of depolarization and backpropagation for LTP & LTD. It also seems plausible given the reported time course of intrinsic plasticity in mammalian systems resulting from learning tasks. As noted in the examples above, rarely is the time course of plasticity the same as that of memory. In some cases, intrinsic excitability is altered during the learning process itself but returns to baseline even as the memory is retained, suggesting that it played a gating or permissive role. In others, intrinsic excitability remains altered even after the memory has been extinguished – possibly to facilitate re-learning (or what is called “savings”).

Homeostatic regulation

One role for which intrinsic plasticity is well-suited is homeostatic regulation, keeping networks subject to Hebbian plasticity and developmental change within workable bounds. The (relatively) slow time scales at which neurons respond to perturbations of background activity suggest intrinsic plasticity is well-suited to serve this regulatory function. An important question is: what exactly is being regulated? In the simplest case, the answer would be average firing rate. Most in vitro experiments on intrinsic plasticity to date have relied on manipulations of average background activity. But experiments in crustacean preparations suggest that the pattern of firing (e.g., bursts versus tonic firing) may also be preserved by intrinsic plasticity. Another intriguing idea is that intrinsic properties are tuned to produce the best match with whatever synaptic input a neuron receives – for example, to allow the neuron to exploit its full dynamic range of firing rates when coding for a given set of inputs (Stemmler and Koch, 1999).

One common, if underexplored, instance of homeostatic regulation in vivo in mammals is an adaptive response to a gene knockout or a transgenic manipulation. To cite one example, when a tonic inhibition received by cerebellar granule cells was eliminated by knockout of the GABA receptor involved, a leak potassium conductance was upregulated so as to exactly compensate (in terms of neuronal behavior) for the loss (Brickley et al., 2001). To cite another, knocking out a calcium channel crucial for pacemaking in dopamine-containing neurons of substantia nigra pars compacta was compensated by a shift in the voltage-dependence of a hyperpolarization-activated cation conductance, which restored pacemaking (Chan et al., 2007).

Disruption of intrinsic plasticity

A disruption of the rules that determine the types of intrinsic plasticity may play a role in disease. Two examples are epilepsies and chronic pain. Epilepsy is a condition where networks of neurons become synchronously active which produces epileptic seizures. This synchrony is mediated in part by pathologies of synaptic contacts but is also mediated by pathologies of intrinsic excitability. Intrinsic excitability plays a critical role in the ascending pathway to signal pain. In the case of chronic injury, intrinsic plasticity can lead to an increased sensitivity to previously innoxious stimuli (hyperalgesia) and to a perception of pain after the noxious stimuli is removed (paresthesia). An understanding of the rules that determine the plasticity of intrinsic excitability, and when it goes wrong, will be a key component to understanding how to treat both epilepsies and chronic pain.

References

Aizenman CD, Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3:109-111.

Aizenman CD, Akerman CJ, Jensen KR, Cline HT (2003) Visually driven regulation of intrinsic neuronal excitability improves stimulus detection in vivo. Neuron 39:831-842.

Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037-1045.

Alkon DL, Lederhendler I, Shoukimas JJ (1982) Primary changes of membrane currents during retention of associative learning. Science 215:693-695.

Antonov I, Antonova I, Kandel ER, Hawkins RD (2001) The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J Neurosci 21:6413-6422.

Armano S, Rossi P, Taglietti V, D'Angelo E (2000) Long-term potentiation of intrinsic excitability at the mossy fiber- granule cell synapse of rat cerebellum. J Neurosci 20:5208-5216.

Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.

Brembs B, Lorenzetti FD, Reyes FD, Baxter DA, Byrne JH (2002) Operant reward learning in Aplysia: neuronal correlates and mechanisms. Science 296:1706-1709.

Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88-92.

Brons JF, Woody CD (1980) Long-term changes in excitability of cortical neurons after Pavlovian conditioning and extinction. J. Neurophysiol. 44:605-615.

Chan CS, Guzman JN, Ilijic E, Mercer JN, Rick C, Tkatch T, Meredith GE, Surmeier DJ (2007) "Rejuvenation" protects neurons in mouse models of Parkinson's disease. Nature 447:1081-1086.

Chavez-Noriega LE, Halliwell JV, Bliss TV (1990) A decrease in firing threshold observed after induction of the EPSP- spike (E-S) component of long-term potentiation in rat hippocampal slices. Exp Brain Res 79:633-641.

Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18:5988-5998.

Cudmore RH, Turrigiano GG (2004) Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J Neurophysiol 92:341-348.

Daoudal G, Hanada Y, Debanne D (2002) Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 99:14512-14517.

Desai NS, Rutherford LC, Turrigiano GG (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2:515-520.

Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83:2733-2737.

Disterhoft JF, Golden DT, Read HL, Coulter DA, Alkon DL (1988) AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res 462:118-125.

Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.

Frick A, Johnston D (2005) Plasticity of dendritic excitability. J Neurobiol 64:100-115.

Gainutdinov KL, Chekmarev LJ, Gainutdinova TH (1998) Excitability increase in withdrawal interneurons after conditioning in snail. Neuroreport 9:517-520.

Gandhi CC, Matzel LD (2000) Modulation of presynaptic action potential kinetics underlies synaptic facilitation of type B photoreceptors after associative conditioning in Hermissenda. Journal of Neuroscience 20:2022-2035.

Haedo R. Golowasch J. (2006) Ionic Mechanism Underlying Recovery of Rhythmic Activity in Adult Isolated Neurons. J Neurophysiol 96:1860-1876.

Kim J, Jung SC, Clemens AM, Petralia RS, Hoffman DA (2007) Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54:933-947.

Li CY, Lu JT, Wu CP, Duan S, Poo MM (2004) Bidirectional modification of presynaptic neuronal excitability accompanying spike timing-dependent synaptic plasticity. Neuron 41:257-268.

Nelson AB, Krispel CM, Sekirnjak C, du Lac S (2003) Long-lasting increases in intrinsic excitability triggered by inhibition. Neuron 40:609-620.

Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF (2003) Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 90:2171-2179.

Rosenkranz JA, Grace AA (2002) Dopamine-mediated modulation of odour-evoked amygdala potentials during Pavlovian conditioning. Nature 417:282-287.

Saar D, Grossman Y, Barkai E (1998) Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10:1518-1523.

Stemmler M, Koch C (1999) How voltage-dependent conductances can adapt to maximize the information encoded by neuronal firing rate. Nat Neurosci 2:521-527.

Tsubokawa H, Offermanns S, Simon M, Kano M (2000) Calcium-dependent persistent facilitation of spike backpropagation in the CA1 pyramidal neurons. J Neurosci 20:4878-4884.

Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977.

Van Welie I, Van Hooft JA, Wadman WJ (2004) Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolization-activated Ih channels. Proc Natl Acad Sci USA 101:5123-5128.

Van Welie I, Van Hooft JA, Wadman WJ (2006) Background activity regulates excitability of rat hippocampal CA1 pyramidal neurons by adaptation of a K+ conductance. J Neurophysiol 95:2007-2012.

Xu J, Kang N, Jiang L, Nedergaard M, Kang J (2005) Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 25:1750-1760.

Xu NL, Ye CQ, Poo MM, Zhang XH (2006) Coincidence detection of synaptic inputs is facilitated at the distal dendrites after long-term potentiation induction. J Neurosci 26:3002-3009.

Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885-900.

Internal references

• Joseph E. LeDoux (2008) Amygdala. Scholarpedia, 3(4):2698.

• Peter Redgrave (2007) Basal ganglia. Scholarpedia, 2(6):1825.

• Valentino Braitenberg (2007) Brain. Scholarpedia, 2(11):2918.

• Eugene M. Izhikevich (2006) Bursting. Scholarpedia, 1(3):1300.

• Nestor A. Schmajuk (2008) Classical conditioning. Scholarpedia, 3(3):2316.

• Gregoire Nicolis and Catherine Rouvas-Nicolis (2007) Complex systems. Scholarpedia, 2(11):1473.

• Howard Eichenbaum (2008) Memory. Scholarpedia, 3(3):1747.

• Peter Jonas and Gyorgy Buzsaki (2007) Neural inhibition. Scholarpedia, 2(9):3286.

• Wolfram Schultz (2007) Reward. Scholarpedia, 2(3):1652.

• Allen Selverston (2008) Stomatogastric ganglion. Scholarpedia, 3(4):1661.

• Arkady Pikovsky and Michael Rosenblum (2007) Synchronization. Scholarpedia, 2(12):1459.

• Kathleen Cullen and Soroush Sadeghi (2008) Vestibular system. Scholarpedia, 3(1):3013.

See also

Homeostatic Plasticity, Gain Modulation, Synaptic Plasticity

Sponsored by: Eugene M. Izhikevich, Editor-in-Chief of Scholarpedia, the peer-reviewed open-access encyclopedia

Reviewed by: Anonymous

Reviewed by: Dr. Jorge Golowasch, NJIT/ Rutgers University, NJ

Accepted on: 2008-02-17 09:07:30 GMT