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Axo-axonic synapse

An axo-axonic synapse is a type of synapse, formed by one neuron projecting its axon terminals onto another neuron's axon.

Background
Complex interconnections of neurons form neural networks, which are responsible for various types of computation in the brain. Neurons receive inputs mainly through dendrites, which play a role in spatio-temporal computation, leading to the firing of an action potential which subsequently travels to synaptic terminals passing through axons. Based on their locations, synapses can be classified into various kinds, such as axo-dendritic synapse, axo-somatic synapse, and axo-axonal synapse. The prefix here indicates the part of the presynaptic neuron (i.e., ‘axo-’ for axons), and the suffix represents the location where the synapse is formed on the postsynaptic neuron (i.e., ‘-dendritic’ for dendrites, ‘-somatic’ for cell body and ‘-axonic’ for synapses on axons). Synapse location will govern the role of that synapse in a network of neurons. In axo-dendritic synapses, the presynaptic activity will affect the spatio-temporal computation in postsynaptic neurons by altering electrical potential in the dendritic branch. Whereas the axo-somatic synapse will affect the probability of firing an action potential in the postsynaptic neuron by causing inhibitory or excitatory effects directly at the cell body. Whereas the other types of synapses modulate postsynaptic neural activity, the axo-axonic synapses show subtle effects on the network-level neural information transfer. In such synapses, the activity in presynaptic neurons will not change the membrane potential (i.e., depolarize or hyperpolarize) of the cell body of postsynaptic neurons because presynaptic neurons project directly on the axons of the postsynaptic neurons. Thus, the axo-axonic synapse will mainly affect the probability of neurotransmitter vesicle release in response to an action potential firing in the postsynaptic neuron. Unlike other kinds of synapses, the axo-axonic synapse manipulates the effects of a postsynaptic neuron's firing on the neurons further downstream in the network. Due to the mechanism of how axo-axonic synapses work, most of these synapses are inhibitory, and yet a few show excitatory effects in postsynaptic neurons. == History ==
History
The first direct evidence of the existence of axo-axonic synapses was provided by E. G. Gray in 1962. Gray produced electron microscopy photographs of axo-axonic synapses formed on the terminals of muscle afferents involved in the spinal somatic reflex arc in a cat's spinal cord slices. Later, Gray coined the term ‘axo-axonic’ after getting photographic confirmation from as many as twelve axo-axonic synapses. Within the next two years, scientists found axo-axonic synapses in various other places in the nervous system in different animals, such as in the retina of cats and pigeons, in the lateral geniculate nucleus of monkeys, in the olfactory bulb of mice, and in various lobes in the octopus brain. This further confirmed the existence of axo-axonic synapses in the brain across animal phyla. Prior to the discovery of axo-axonic synapses, physiologists predicted the possibility of such mechanisms as early as in year 1935, following their observations of electrophysiological recordings and quantal analysis of brain segments. They had observed inhibitory responses in postsynaptic motoneurons in the slice preparation of the monosynaptic reflex arc. During simultaneous recordings from presynaptic and postsynaptic neurons, the physiologists could not make sense of the infrequent inhibition observed in the postsynaptic neuron, with no membrane potential changes in the presynaptic neuron. At that time, this phenomenon was known as “presynaptic inhibitory action”, the term proposed by Karl Frank in 1959 and later well summarized by John Eccles in his book. After Gray's finding of the axo-axonic synapse in 1962, scientists confirmed that this phenomenon was in fact due to the axo-axonic synapse present in the reflex arc. More recently, in 2006 researchers discovered the first evidence of excitatory effects caused by an axo-axonic synapse. They found that GABAergic neurons project onto the axons of pyramidal cells in the cerebral cortex to form axo-axonic synapse and elicit excitatory effects in cortical microcircuits. == Function ==
Function
Below are the brain locations where axo-axonic synapses are found in different animals. Cerebellar cortex The axo-axonic synapse in the cerebellar cortex originally appeared in one of the drawings of Santiago Ramón y Cajal in his book published in 1909. Later using electron microscopy, it was confirmed that the basket cell axon projects on the axon hillock of Purkinje cells in the cerebellar cortex in cats and other mammals, forming axo-axonic synapses. Network-level study revealed that the granule cells which, through their parallel fibers, activate Purkinje cells, also activate the basket cells, which subsequently inhibit the effect of Purkinje cells on the downstream network. Cerebral cortex Axo-axonic synapses are found In the visual cortex (in V1 and V2) in mammals, and have been well studied in cats, rats and primates such as monkeys. The synapse is formed on the initial segments of the axons of pyramidal cells in several layers in the visual cortex. The projecting neurons for these synapses come from various parts of the central nervous system and neocortex. Similarly, axo-axonic synapses are found in the motor cortex, in the subiculum and in the piriform cortex. Studying the locations of axo-axonic synapses in the primary olfactory cortex, researchers have suggested that axo-axonic synapses may play a critical role in synchronizing oscillations in the piriform cortex (in the olfactory cortex), which aids olfaction. The axo-axonic synapses are also found in the hippocampus. These synapses are found to be formed mainly on principal cells in stratum oriens and stratum pyramidale and rarely on stratum radiatum; they commonly receive projections from GABAergic local interneurons. The horizontal interneurons show a laminar distribution of dendrites and are involved in axo-axonic synapses in the hippocampus, which get direct synaptic inputs from CA1 pyramidal cells. In this study, authors examined 4,811 synapses in rat striatum sections, and 15 of them were found to be the axo-axonic synapses. These axo-axonic synapses are formed by dopaminergic inhibitory interneurons (on the presynaptic side) projecting onto the axons of glutamatergic cortico-striatal fibers in the rat striatum. Electron microscopy studies on the kitten brainstem quantified synaptogenesis of axo-axonic synapses in the spinal trigeminal nucleus at different development ages of the brain. Authors identified the synapses by counting vesicles released in the synaptic cleft, which can be observed in the micrographs. Axo-axonic contacts are shown to consistently increase throughout the development period, starting from the age of 3 hours to the age of 27 days in kittens. The highest rate of synaptogenesis is during the first 3 to 6 days, at the end of which, the kitten's spinal trigeminal nucleus will have nearly half of the axo-axonic synapses present in adult cats. Later, between 16 and 27 days of age, there is another surge of axo-axonic synaptogenesis. Spinal Cord Axo-axonic synapses are found in the mammalian spinal reflex arc and in Substantia gelatinosa of Rolando (SGR). In the spinal cord, axo-axonic synapses are formed on the terminals of sensory neurons with presynaptic inhibitory interneurons. These synapses are first studied using intracellular recordings from the spinal motoneurons in cats, and have been shown to cause presynaptic inhibition. This seems to be a common mechanism in spinal cords, in which GABAergic interneurons inhibit presynaptic activity in sensory neurons and eventually control activity in motor neurons enabling selective control of muscles. In efforts to quantify the occurrence of axo-axonic synapses in the SGR region in rats, 54 such synapses were found among the total 6,045 synapses examined. These 54 axo-axonic synapses were shown to have either agranular vesicles or large granular vesicles. Interestingly, the authors claimed that axo-axonic synapses, which are abundant in rats, are absent in the lateral vestibular nucleus in cats. The axon hillock and initial axon segments of mauthner cells receive terminals from extremely fine unmyelinated fibers, which cover the axon hillock with helical projections. These helical projections around mauthner cells are also known as the axon cap. The difference between the axo-axonic synapses and other synapses on mauthner cells is that synapses on dendrites and soma receive myelinated fibers, while axons receive unmyelinated fibers. Neuromuscular junction Inhibitory axo-axonic synapses are found in the crustacean neuromuscular junctions and have been widely studied in Crayfish. Axo-axonic synapses are formed on the excitatory axons as a postsynaptic neuron by the motor neurons from the presynaptic side. Motor neurons, which is the common inhibitor in crab limb closers and limb accessory flexors, form axo-axonic synapses in addition to the neuromuscular junction with the muscles in crayfish. These synapses were first observed in 1967, when they were found to cause presynaptic inhibition in leg muscles of crayfish and crabs. Subsequent studies found that axo-axonic synapses showed varying numbers of occurrence based on the location of the leg muscles from the nervous system. For instance, proximal regions have thrice as many axo-axonic synapses than the central regions. These synapses are proposed to function by limiting neurotransmitter release for controlled leg movements. == Clinical Significance ==
Clinical Significance
An example of the physiological role of axo-axonic synapses, which are formed by GABAergic inhibitory interneurons to the axons of granule cells, is in eliciting spontaneous seizures, which is a key symptom of Intractable Epilepsy. The presynaptic inhibitory interneurons, which can be labeled by cholecystokinin and GAT-1, are found to modulate the granule cells's spike output. The same cells subsequently project excitatory mossy fibers to pyramidal neurons in the hippocampal CA3 region. One of the two leading theories for the pathoetiology of schizophrenia is the glutamate theory. Glutamate is a well studied neurotransmitter for its role in learning and memory, and also in the brain development during prenatal and childhood. Studies of rat striatum found inhibitory axo-axonic synapses formed on the glutamatergic cortico-striatal fibers. This mechanism is proposed to be a possible mechanism for glutamate dysfunction in observed schizophrenia. == Development ==
Development
A study on the spinal cord in mice suggests that the sensory Ig/Caspr4 complex is involved in the formation of axo-axonic synapses on proprioceptive afferents. These synapses are formed through projection of GABAergic interneurons on sensory neurons, which is upstream to the motor neurons. In the axo-axonic synapse, expressing NB2 (Contactin5)/Caspr4 coreceptor complex in postsynaptic neurons along with expressing NrCAM/CHL1 in presynaptic interneurons results in the increased numbers of such synapses forming in the spinal cord. == See also ==
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