Long-term depression


In neurophysiology, long-term depression is an activity-dependent reduction in the efficacy of neuronal synapses lasting hours or longer following a long patterned stimulus. LTD occurs in many areas of the CNS with varying mechanisms depending upon brain region and developmental progress.
As the opposing process to long-term potentiation, LTD is one of several processes that serves to selectively weaken specific synapses in order to make constructive use of synaptic strengthening caused by LTP. This is necessary because, if allowed to continue increasing in strength, synapses would ultimately reach a ceiling level of efficiency, which would inhibit the encoding of new information. Both LTD and LTP are forms of synaptic plasticity.

Characterisation

LTD in the hippocampus and cerebellum have been the best characterized, but there are other brain areas in which mechanisms of LTD are understood. LTD has also been found to occur in different types of neurons that release various neurotransmitters, however, the most common neurotransmitter involved in LTD is L-glutamate. L-glutamate acts on the N-methyl-D-aspartate receptors, α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors, kainate receptors, and metabotropic glutamate receptors during LTD. It can result from strong synaptic stimulation or from persistent weak synaptic stimulation. Long-term potentiation is the opposing process to LTD; it is the long-lasting increase of synaptic strength. In conjunction, LTD and LTP are factors affecting neuronal synaptic plasticity. LTD is thought to result mainly from a decrease in postsynaptic receptor density, although a decrease in presynaptic neurotransmitter release may also play a role. Cerebellar LTD has been hypothesized to be important for motor learning. However, it is likely that other plasticity mechanisms play a role as well. Hippocampal LTD may be important for the clearing of old memory traces.
Hippocampal/cortical LTD can be dependent on NMDA receptors, metabotropic glutamate receptors, or endocannabinoids. The result of the underlying-LTD molecular mechanism in cerebellum is the phosphorylation of AMPA glutamate receptors and their elimination from the surface of the parallel fiber-Purkinje cell synapse.

Neural homeostasis

It is highly important for neurons to maintain a variable range of neuronal output. If synapses were only reinforced by positive feedback, they would eventually come to the point of complete inactivity or too much activity. To prevent neurons from becoming static, there are two regulatory forms of plasticity that provide negative feedback: metaplasticity and scaling. Metaplasticity is expressed as a change in the capacity to provoke subsequent synaptic plasticity, including LTD and LTP. The Bienenstock, Cooper and Munro model proposes that a certain threshold exists such that a level of postsynaptic response below the threshold leads to LTD and above it leads to LTP. BCM theory further proposes that the level of this threshold depends upon the average amount of postsynaptic activity. Scaling has been found to occur when the strength of all of a neuron's excitatory inputs are scaled up or down. LTD and LTP coincide with metaplasticity and synaptic scaling to maintain proper neuronal network function.

General forms of LTD

Long-term depression can be described as either homosynaptic plasticity or heterosynaptic plasticity. Homosynaptic LTD is restricted to the individual synapse that is activated by a low frequency stimulus. In other words, this form of LTD is activity-dependent, because the events causing the synaptic weakening occur at the same synapse that is being activated. Homosynaptic LTD is also associative in that it correlates the activation of the postsynaptic neuron with the firing of the presynaptic neuron. Heterosynaptic LTD, in contrast, occurs at synapses that are not potentiated or are inactive. The weakening of a synapse is independent of the activity of the presynaptic or postsynaptic neurons as a result of the firing of a distinct modulatory interneuron. Thus, this form of LTD impacts synapses nearby those receiving action potentials.

Mechanisms that weaken synapses

Hippocampus

LTD affects hippocampal synapses between the Schaffer collaterals and the CA1 pyramidal cells. LTD at the Schaffer collateral-CA1 synapses depends on the timing and frequency of calcium influx. LTD occurs at these synapses when Schaffer collaterals are stimulated repetitively for extended time periods at a low frequency. Depressed excitatory postsynaptic potentials result from this particular stimulation pattern. The magnitude of calcium signal in the postsynaptic cell largely determines whether LTD or LTP occurs. NMDA-receptor dependent LTD is induced by moderate rises in postsynaptic calcium levels. The threshold level in area CA1 is on a sliding scale that depends on the history of the synapse. If the synapse has already been subject to LTP, the threshold is raised, increasing the probability that a calcium influx will yield LTD. In this way, a "negative feedback" system maintains synaptic plasticity. Activation of NMDA-type glutamate receptors, which belong to a class of ionotropic glutamate receptors, is required for calcium entry into the CA1 postsynaptic cell. Change in voltage provides a graded control of postsynaptic Ca2+ by regulating NMDAR-dependent Ca2+ influx, which is responsible for initiating LTD.
While LTP is in part due to the activation of protein kinases, which subsequently phosphorylate target proteins, LTD arises from activation of calcium-dependent phosphatases that dephosphorylate the target proteins. Selective activation of these phosphatases by varying calcium levels might be responsible for the different effects of calcium observed during LTD. The activation of postsynaptic phosphatases causes internalization of synaptic AMPA receptors into the postsynaptic cell by clathrin-coated endocytosis mechanisms, thereby reducing sensitivity to glutamate released by Schaffer collateral terminals.

Cerebellum

LTD occurs at synapses in cerebellar Purkinje neurons, which receive two forms of excitatory input, one from a single climbing fiber and one from hundreds of thousands of parallel fibers. LTD decreases the efficacy of parallel fiber synapse transmission, though, according to recent findings, it also impairs climbing fiber synapse transmission. Both parallel fibers and climbing fibers must be simultaneously activated for LTD to occur. With respect to calcium release however, it is best if the parallel fibers are activated a few hundred milliseconds before the climbing fibres. In one pathway, parallel fiber terminals release glutamate to activate AMPA and metabotropic glutamate receptors in the postsynaptic Purkinje cell. When glutamate binds to the AMPA receptor, the membrane depolarizes. Glutamate binding to the metabotropic receptor activates phospholipase C and produces diacylglycerol and inositol triphosphate second messengers. In the pathway initiated by activation of climbing fibers, calcium enters the postsynaptic cell through voltage-gated ion channels, raising intracellular calcium levels. Together, DAG and IP3 augment the calcium concentration rise by targeting IP3-sensitive receptors triggering release of calcium from intracellular stores as well as protein kinase C activation. PKC phosphorylates AMPA receptors, which promotes their dissociation from scaffold proteins in the post-synaptic membrane and subsequent internalization. With the loss of AMPA receptors, the postsynaptic Purkinje cell response to glutamate release from parallel fibers is depressed. Calcium triggering in the cerebellum is a critical mechanism involved in long-term depression. Parallel fibre terminals and climbing fibres work together in a positive feedback loop for invoking high calcium release. LTD is involved in predictive control exerted by cerebellar circuitry and cerebellar reserve.

Ca2+ involvement

Further research has determined calcium's role in long-term depression induction. While other mechanisms of long-term depression are being investigated, calcium's role in LTD is a defined and well understood mechanism by scientists. High calcium concentrations in the post-synaptic Purkinje cells is a necessity for the induction of long-term depression. There are several sources of calcium signaling that elicit LTD: climbing fibres and parallel fibres which converge onto Purkinje cells. Calcium signaling in the post-synaptic cell involved both spatial and temporal overlap of climbing fibre induced calcium release into dendrites as well as parallel fibre induced mGluRs and IP3 mediated calcium release. In the climbing fibres, AMPAR-mediated depolarization induces a regenerative action potential that spreads to the dendrites, which is generated by voltage-gated calcium channels. Paired with PF-mediated mGluR1 activation results in LTD induction. In the parallel fibres, GluRs are activated by constant activation of the parallel fibres which indirectly induces the IP3 to bind to its receptor and activate calcium release from intracellular storage. In calcium induction, there is a positive feedback loop to regenerate calcium for long-term depression. Climbing and parallel fibres must be activated together to depolarize the Purkinje cells while activating mGlur1s. Timing is a critical component to CF and PF as well, a better calcium release involves PF activation a few hundred milliseconds before CF activity.

AMPAR phosphorylation

There is a series of signaling cascades, MAPK, in the cerebellum that plays a critical role in cerebellum LTD. The MAPK cascade is important in information processing within neurons and other various types of cells. The cascade includes MAPKKK, MAPKK, and MAPK. Each is dual phosphorylated by the other, MAPKKK dual phosphorylates MAPKK and in turn dual phosphorylates MAPK. There is a positive feedback loop that results from a simultaneous input of signals from PF-CF and increases DAG and Ca2+ in Purkinje dendritic spines. Calcium and DAG activate conventional PKC, which then activates MAPKKK and the rest of the MAPK cascade. Activated MAPK and Ca2+ activate PLA2, AA and cPKC creating a positive feedback loop. Induced cPKC phosphorylates AMPA receptors and are eventually removed from the postsynaptic membrane via endocytosis. The timescale is for this process is approximately 40 minutes. Overall, the magnitude of the LTD correlates with AMPAR phosphorylation.