Autapse

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An autapse is a chemical or electrical synapse from a neuron onto itself. [1] [2] It can also be described as a synapse formed by the axon of a neuron on its own dendrites, in vivo or in vitro .

Contents

History

The term "autapse" was first coined in 1972 by Van der Loos and Glaser, who observed them in Golgi preparations of the rabbit occipital cortex while originally conducting a quantitative analysis of neocortex circuitry. [3] Also in the 1970s, autapses have been described in dog and rat cerebral cortex, [4] [5] [6] monkey neostriatum, [7] and cat spinal cord. [8]

In 2000, they were first modeled as supporting persistence in recurrent neural networks. [1] In 2004, they were modeled as demonstrating oscillatory behavior, which was absent in the same model neuron without autapse. [9] More specifically, the neuron oscillated between high firing rates and firing suppression, reflecting the spike bursting behavior typically found in cerebral neurons. In 2009, autapses were, for the first time, associated with sustained activation. This proposed a possible function for excitatory autapses within a neural circuit. [10] In 2014, electrical autapses were shown to generate stable target and spiral waves in a neural model network. [11] This indicated that they played a significant role in stimulating and regulating the collective behavior of neurons in the network. In 2016, a model of resonance was offered. [12]

Autapses have been used to simulate "same cell" conditions to help researchers make quantitative comparisons, such as studying how N-methyl-D-aspartate receptor (NMDAR) antagonists affect synaptic versus extrasynaptic NMDARs. [13]

Formation

Recently, it has been proposed that autapses could possibly form as a result of neuronal signal transmission blockage, such as in cases of axonal injury induced by poisoning or impeding ion channels. [14] Dendrites from the soma in addition to an auxiliary axon may develop to form an autapse to help remediate the neuron's signal transmission.

Structure and function

Autapses can be either glutamate-releasing (excitatory) or GABA-releasing (inhibitory), just like their traditional synapse counterparts. [15] Similarly, autapses can be electrical or chemical by nature. [2]

Broadly speaking, negative feedback in autapses tends to inhibit excitable neurons whereas positive feedback can stimulate quiescent neurons. [16]

Although the stimulation of inhibitory autapses did not induce hyperpolarizing inhibitory post-synaptic potentials in interneurons of layer V of neocortical slices, they have been shown to impact excitability. [17] Upon using a GABA-antagonist to block autapses, the likelihood of an immediate subsequent second depolarization step increased following a first depolarization step. This suggests that autapses act by suppressing the second of two closely timed depolarization steps and therefore, they may provide feedback inhibition onto these cells. This mechanism may also potentially explain shunting inhibition.

In cell culture, autapses have been shown to contribute to the prolonged activation of B31/B32 neurons, which significantly contribute food-response behavior in Aplysia . [10] This suggests that autapses may play a role in mediating positive feedback. The B31/B32 autapse was unable to play a role in initiating the neuron's activity, although it is believed to have helped sustain the neuron's depolarized state. The extent to which autapses maintain depolarization remains unclear, particularly since other components of the neural circuit (i.e. B63 neurons) are also capable of providing strong synaptic input throughout the depolarization. Additionally, it has been suggested that autapses provide B31/B32 neurons with the ability to quickly repolarize. Bekkers (2009) has proposed that specifically blocking the contribution of autapses and then assessing the differences with or without blocked autapses could better illuminate the function of autapses. [18]

Hindmarsh–Rose (HR) model neurons have demonstrated chaotic, regular spiking, quiescent, and periodic patterns of burst firing without autapses. [19] Upon the introduction of an electrical autapse, the periodic state switches to the chaotic state and displays an alternating behavior that increases in frequency with a greater autaptic intensity and time delay. On the other hand, excitatory chemical autapses enhanced the overall chaotic state. The chaotic state was reduced and suppressed in the neurons with inhibitory chemical autapses. In HR model neurons without autapses, the pattern of firing altered from quiescent to periodic and then to chaotic as DC current was increased. Generally, HR model neurons with autapses have the ability to swap into any firing pattern, regardless of the prior firing pattern.

Location

Neurons from several brain regions, such as the neocortex, substantia nigra, and hippocampus have been found to contain autapses. [3] [20] [21] [22]

Autapses have been observed to be relatively more abundant in GABAergic basket and dendrite-targeting cells of the cat visual cortex compared to spiny stellate, double bouquet, and pyramidal cells, suggesting that the degree of neuron self-innervation is cell-specific. [23] Additionally, dendrite-targeting cell autapses were, on average, further from the soma compared to basket cell autapses.

80% of layer V pyramidal neurons in developing rat neocortices contained autaptic connections, which were located more so on basal dendrites and apical oblique dendrites rather than main apical dendrites. [24] The dendritic positions of synaptic connections of the same cell type were similar to those of autapses, suggesting that autaptic and synaptic networks share a common mechanism of formation.

Disease implications

In the 1990s, paroxysmal depolarizing shift-type interictal epileptiform discharges has been suggested to be primarily dependent on autaptic activity for solitary excitatory hippocampal rat neurons grown in microculture. [25]

More recently, in human neocortical tissues of patients with intractable epilepsy, the GABAergic output autapses of fast-spiking (FS) neurons have been shown to have stronger asynchronous release (AR) compared to both non-epileptic tissue and other types of synapses involving FS neurons. [26] The study found similar results using a rat model as well. An increase in residual Ca2+ concentration in addition to the action potential amplitude in FS neurons was suggested to cause this increase in AR of epileptic tissue. Anti-epileptic drugs could potentially target this AR of GABA that seems to rampantly occur at FS neuron autapses.

Effects of drugs

Using a glia-conditioned medium to treat glia-free purified rat retinal ganglion microcultures has been shown to significantly increase the number of autapses per neuron compared to a control. [27] This suggests that glia-derived soluble, proteinase K-sensitive factors induce autapse formation in rat retinal ganglion cells.

Related Research Articles

<span class="mw-page-title-main">Dendrite</span> Small projection on a neuron that receives signals

A dendrite or dendron is a branched protoplasmic extension of a nerve cell that propagates the electrochemical stimulation received from other neural cells to the cell body, or soma, of the neuron from which the dendrites project. Electrical stimulation is transmitted onto dendrites by upstream neurons via synapses which are located at various points throughout the dendritic tree.

<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">Electrical synapse</span> Type of connection between neurons

An electrical synapse is a mechanical and electrically conductive synapse, a functional junction between two neighboring neurons. The synapse is formed at a narrow gap between the pre- and postsynaptic neurons known as a gap junction. At gap junctions, such cells approach within about 3.8 nm of each other, a much shorter distance than the 20- to 40-nanometer distance that separates cells at a chemical synapse. In many animals, electrical synapse-based systems co-exist with chemical synapses.

<span class="mw-page-title-main">Olfactory bulb</span> Neural structure

The olfactory bulb is a neural structure of the vertebrate forebrain involved in olfaction, the sense of smell. It sends olfactory information to be further processed in the amygdala, the orbitofrontal cortex (OFC) and the hippocampus where it plays a role in emotion, memory and learning. The bulb is divided into two distinct structures: the main olfactory bulb and the accessory olfactory bulb. The main olfactory bulb connects to the amygdala via the piriform cortex of the primary olfactory cortex and directly projects from the main olfactory bulb to specific amygdala areas. The accessory olfactory bulb resides on the dorsal-posterior region of the main olfactory bulb and forms a parallel pathway. Destruction of the olfactory bulb results in ipsilateral anosmia, while irritative lesions of the uncus can result in olfactory and gustatory hallucinations.

An inhibitory postsynaptic potential (IPSP) is a kind of synaptic potential that makes a postsynaptic neuron less likely to generate an action potential. 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. EPSPs and IPSPs compete with each other at numerous synapses of a neuron. This determines whether an action potential occurring at the presynaptic terminal produces an action potential at the postsynaptic membrane. Some common neurotransmitters involved in IPSPs are GABA and glycine.

<span class="mw-page-title-main">Pyramidal cell</span> Projection neurons in the cerebral cortex and hippocampus

Pyramidal cells, or pyramidal neurons, are a type of multipolar neuron found in areas of the brain including the cerebral cortex, the hippocampus, and the amygdala. Pyramidal cells are the primary excitation units of the mammalian prefrontal cortex and the corticospinal tract. One of the main structural features of the pyramidal neuron is the conic shaped soma, or cell body, after which the neuron is named. Other key structural features of the pyramidal cell are a single axon, a large apical dendrite, multiple basal dendrites, and the presence of dendritic spines.

<span class="mw-page-title-main">Nigrostriatal pathway</span> Bilateral pathway in the brain

The nigrostriatal pathway is a bilateral dopaminergic pathway in the brain that connects the substantia nigra pars compacta (SNc) in the midbrain with the dorsal striatum in the forebrain. It is one of the four major dopamine pathways in the brain, and is critical in the production of movement as part of a system called the basal ganglia motor loop. Dopaminergic neurons of this pathway release dopamine from axon terminals that synapse onto GABAergic medium spiny neurons (MSNs), also known as spiny projection neurons (SPNs), located in the striatum.

Schaffer collaterals are axon collaterals given off by CA3 pyramidal cells in the hippocampus. These collaterals project to area CA1 of the hippocampus and are an integral part of memory formation and the emotional network of the Papez circuit, and of the hippocampal trisynaptic loop. It is one of the most studied synapses in the world and named after the Hungarian anatomist-neurologist Károly Schaffer.

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">Stellate cell</span>

Stellate cells are neurons in the central nervous system, named for their star-like shape formed by dendritic processes radiating from the cell body. Many stellate cells are GABAergic and are located in the molecular layer of the cerebellum. Stellate cells are derived from dividing progenitor cells in the white matter of postnatal cerebellum. Dendritic trees can vary between neurons. There are two types of dendritic trees in the cerebral cortex, which include pyramidal cells, which are pyramid shaped and stellate cells which are star shaped. Dendrites can also aid neuron classification. Dendrites with spines are classified as spiny, those without spines are classified as aspinous. Stellate cells can be spiny or aspinous, while pyramidal cells are always spiny. Most common stellate cells are the inhibitory interneurons found within the upper half of the molecular layer in the cerebellum. Cerebellar stellate cells synapse onto the dendritic trees of Purkinje cells and send inhibitory signals. Stellate neurons are sometimes found in other locations in the central nervous system; cortical spiny stellate cells are found in layer IVC of the primary visual cortex. In the somatosensory barrel cortex of mice and rats, glutamatergic (excitatory) spiny stellate cells are organized in the barrels of layer 4. They receive excitatory synaptic fibres from the thalamus and process feed forward excitation to 2/3 layer of the primary visual cortex to pyramidal cells. Cortical spiny stellate cells have a 'regular' firing pattern. Stellate cells are chromophobes, that is cells that does not stain readily, and thus appears relatively pale under the microscope.

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

In neuroscience, Golgi cells are the most abundant inhibitory interneurons found within the granular layer of the cerebellum. Golgi cells can be found in the granular layer at various layers. The Golgi cell is essential for controlling the activity of the granular layer. They were first identified as inhibitory in 1964. It was also the first example of an inhibitory feedback network in which the inhibitory interneuron was identified anatomically. Golgi cells produce a wide lateral inhibition that reaches beyond the afferent synaptic field and inhibit granule cells via feedforward and feedback inhibitory loops. These cells synapse onto the dendrite of granule cells and unipolar brush cells. They receive excitatory input from mossy fibres, also synapsing on granule cells, and parallel fibers, which are long granule cell axons. Thereby this circuitry allows for feed-forward and feed-back inhibition of granule cells.

<span class="mw-page-title-main">Synapse</span> Structure connecting neurons in the nervous system

In the nervous system, a synapse is a structure that permits a neuron to pass an electrical or chemical signal to another neuron or to the target effector cell.

<span class="mw-page-title-main">Mossy fiber (hippocampus)</span> Pathway in the hippocampus

In the hippocampus, the mossy fiber pathway consists of unmyelinated axons projecting from granule cells in the dentate gyrus that terminate on modulatory hilar mossy cells and in Cornu Ammonis area 3 (CA3), a region involved in encoding short-term memory. These axons were first described as mossy fibers by Santiago Ramón y Cajal as they displayed varicosities along their lengths that gave them a mossy appearance. The axons that make up the pathway emerge from the basal portions of the granule cells and pass through the hilus of the dentate gyrus before entering the stratum lucidum of CA3. Granule cell synapses tend to be glutamatergic, though immunohistological data has indicated that some synapses contain neuropeptidergic elements including opiate peptides such as dynorphin and enkephalin. There is also evidence for co-localization of both GABAergic and glutamatergic neurotransmitters within mossy fiber terminals. GABAergic and glutamatergic co-localization in mossy fiber boutons has been observed primarily in the developing hippocampus, but in adulthood, evidence suggests that mossy fiber synapses may alternate which neurotransmitter is released through activity-dependent regulation.

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

Chandelier cells or chandelier neurons are a subset of GABAergic cortical interneurons. They are described as parvalbumin-containing and fast-spiking to distinguish them from other subtypes of GABAergic neurons, although some studies have suggested that only a subset of chandelier cells test positive for parvalbumin by immunostaining. The name comes from the specific shape of their axon arbors, with the terminals forming distinct arrays called "cartridges". The cartridges are immunoreactive to an isoform of the GABA membrane transporter, GAT-1, and this serves as their identifying feature. GAT-1 is involved in the process of GABA reuptake into nerve terminals, thus helping to terminate its synaptic activity. Chandelier neurons synapse exclusively to the axonal initial segment of pyramidal neurons, near the site where action potential is generated. It is believed that they provide inhibitory input to the pyramidal neurons, but there is data showing that in some circumstances the GABA from chandelier neurons could be excitatory.

Neural backpropagation is the phenomenon in which, after the action potential of a neuron creates a voltage spike down the axon, another impulse is generated from the soma and propagates towards the apical portions of the dendritic arbor or dendrites. In addition to active backpropagation of the action potential, there is also passive electrotonic spread. While there is ample evidence to prove the existence of backpropagating action potentials, the function of such action potentials and the extent to which they invade the most distal dendrites remain highly controversial.

<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.

<span class="mw-page-title-main">Granule cell</span> Type of neuron with a very small cell body

The name granule cell has been used for a number of different types of neurons whose only common feature is that they all have very small cell bodies. Granule cells are found within the granular layer of the cerebellum, the dentate gyrus of the hippocampus, the superficial layer of the dorsal cochlear nucleus, the olfactory bulb, and the cerebral cortex.

Joro spider toxin - a toxin which was originally extracted from the venom of the joro spider, originally native to Japan.

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

Unipolar brush cells (UBCs) are a class of excitatory glutamatergic interneuron found in the granular layer of the cerebellar cortex and also in the granule cell domain of the cochlear nucleus.

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

References

  1. 1 2 Seung, H. Sebastian; Lee, Daniel D.; Reis, Ben Y.; Tank, David W. (2000-09-01). "The Autapse: A Simple Illustration of Short-Term Analog Memory Storage by Tuned Synaptic Feedback". Journal of Computational Neuroscience. 9 (2): 171–185. doi:10.1023/A:1008971908649. ISSN   0929-5313. PMID   11030520. S2CID   547421.
  2. 1 2 Yilmaz, Ergin; Ozer, Mahmut; Baysal, Veli; Perc, Matjaž (2016-08-02). "Autapse-induced multiple coherence resonance in single neurons and neuronal networks". Scientific Reports. 6 (1): 30914. Bibcode:2016NatSR...630914Y. doi:10.1038/srep30914. ISSN   2045-2322. PMC   4969620 . PMID   27480120.
  3. 1 2 Van der Loos, H.; Glaser, E. M. (1972-12-24). "Autapses in neocortex cerebri: synapses between a pyramidal cell's axon and its own dendrites". Brain Research. 48: 355–360. doi:10.1016/0006-8993(72)90189-8. ISSN   0006-8993. PMID   4645210.
  4. ↑ Shkol’nik-Yarros, Ekaterina G. (1971). Neurons and Interneuronal Connections of the Central Visual System | SpringerLink. doi:10.1007/978-1-4684-0715-0. ISBN   978-1-4684-0717-4. S2CID   37317913.
  5. ↑ Preston, R.J.; Bishop, G.A.; Kitai, S.T. (1980-02-10). "Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study". Brain Research. 183 (2): 253–263. doi:10.1016/0006-8993(80)90462-X. ISSN   0006-8993. PMID   7353139. S2CID   1827091.
  6. ↑ Peters, A.; Proskauer, C. C. (April 1980). "Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study". Journal of Neurocytology. 9 (2): 163–183. doi:10.1007/bf01205156. ISSN   0300-4864. PMID   6160209. S2CID   34203892.
  7. ↑ DiFiglia, M.; Pasik, P.; Pasik, T. (1976-09-17). "A Golgi study of neuronal types in the neostriatum of monkeys". Brain Research. 114 (2): 245–256. doi:10.1016/0006-8993(76)90669-7. ISSN   0006-8993. PMID   822916. S2CID   40311354.
  8. ↑ Scheibel, M.E.; Scheibel, A.B. (1971). "Inhibition and the Renshaw Cell A Structural Critique; pp. 73–93". Brain, Behavior and Evolution. 4 (1): 73–93. doi:10.1159/000125425. ISSN   0006-8977.
  9. ↑ Herrmann, Christoph S. (August 2004). "Autapse Turns Neuron Into Oscillator". International Journal of Bifurcation and Chaos. 4 (2): 623–633. Bibcode:2004IJBC...14..623H. doi:10.1142/S0218127404009338.
  10. 1 2 Saada, R.; Miller, N.; Hurwitz, I.; Susswein, A. J. (2009). "Autaptic muscarinic excitation underlies a plateau potential and persistent activity in a neuron of known behavioral function". Current Biology. 19 (6): 479–484. doi: 10.1016/j.cub.2009.01.060 . PMID   19269179. S2CID   15990017.
  11. ↑ Qin, H.; Ma, J.; Wang, C.; Chu, R. (2014). "Autapse-induced target wave, spiral wave in regular network of neurons". Science China Physics, Mechanics & Astronomy. 57 (10): 1918–1926. Bibcode:2014SCPMA..57.1918Q. doi:10.1007/s11433-014-5466-5. S2CID   120661751.
  12. ↑ Yilmaz, E.; Ozer, M.; Baysal, V.; Perc, M. (2 August 2016). "Autapse-induced multiple coherence resonance in single neurons and neuronal networks". Scientific Reports. 9: 30914. Bibcode:2016NatSR...630914Y. doi:10.1038/srep30914. PMC   4969620 . PMID   27480120.
  13. ↑ Xia, Peng; Chen, Huei-sheng Vincent; Zhang, Dongxian; Lipton, Stuart A. (2010-08-18). "Memantine Preferentially Blocks Extrasynaptic over Synaptic NMDA Receptor Currents in Hippocampal Autapses". Journal of Neuroscience. 30 (33): 11246–11250. doi:10.1523/JNEUROSCI.2488-10.2010. ISSN   0270-6474. PMC   2932667 . PMID   20720132.
  14. ↑ Wang, Chunni; Guo, Shengli; Xu, Ying; Ma, Jun; Tang, Jun; Alzahrani, Faris; Hobiny, Aatef (2017). "Formation of Autapse Connected to Neuron and Its Biological Function". Complexity. 2017: 1–9. doi: 10.1155/2017/5436737 . ISSN   1076-2787.
  15. ↑ Ikeda, Kaori; Bekkers, John M. (2006-05-09). "Autapses". Current Biology. 16 (9): R308. doi: 10.1016/j.cub.2006.03.085 . ISSN   0960-9822. PMID   16682332.
  16. ↑ Qin, Huixin; Wu, Ying; Wang, Chunni; Ma, Jun (2015). "Emitting waves from defects in network with autapses". Communications in Nonlinear Science and Numerical Simulation. 23 (1–3): 164–174. Bibcode:2015CNSNS..23..164Q. doi:10.1016/j.cnsns.2014.11.008.
  17. ↑ Bacci, Alberto; Huguenard, John R.; Prince, David A. (2003-02-01). "Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex". The Journal of Neuroscience. 23 (3): 859–866. doi: 10.1523/JNEUROSCI.23-03-00859.2003 . ISSN   1529-2401. PMC   6741939 . PMID   12574414.
  18. ↑ Bekkers, John M. (2009). "Synaptic Transmission: Excitatory Autapses Find a Function?". Current Biology. 19 (7): R296–R298. doi: 10.1016/j.cub.2009.02.010 . PMID   19368875. S2CID   15821336.
  19. ↑ Wang, Hengtong; Ma, Jun; Chen, Yueling; Chen, Yong (2014). "Effect of an autapse on the firing pattern transition in a bursting neuron". Communications in Nonlinear Science and Numerical Simulation. 19 (9): 3242–3254. Bibcode:2014CNSNS..19.3242W. doi:10.1016/j.cnsns.2014.02.018.
  20. ↑ Park, Melburn R.; Lighthall, James W.; Kitai, Stephen T. (1980). "Recurrent inhibition in the rat neostriatum". Brain Research. 194 (2): 359–369. doi:10.1016/0006-8993(80)91217-2. PMID   7388619. S2CID   29451737.
  21. ↑ Karabelas, Athanasios B.; Purrura, Dominick P. (1980). "Evidence for autapses in the substantia nigra". Brain Research. 200 (2): 467–473. doi:10.1016/0006-8993(80)90935-x. PMID   6158366. S2CID   35517474.
  22. ↑ Cobb, S.R; Halasy, K; Vida, I; Nyı́ri, G; Tamás, G; Buhl, E.H; Somogyi, P (1997). "Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus". Neuroscience. 79 (3): 629–648. doi:10.1016/s0306-4522(97)00055-9. PMID   9219929. S2CID   15479304.
  23. ↑ Tamás, G.; Buhl, E. H.; Somogyi, P. (1997-08-15). "Massive autaptic self-innervation of GABAergic neurons in cat visual cortex". The Journal of Neuroscience. 17 (16): 6352–6364. doi: 10.1523/JNEUROSCI.17-16-06352.1997 . ISSN   0270-6474. PMC   6568358 . PMID   9236244.
  24. ↑ Lübke, J.; Markram, H.; Frotscher, M.; Sakmann, B. (1996-05-15). "Frequency and dendritic distribution of autapses established by layer 5 pyramidal neurons in the developing rat neocortex: comparison with synaptic innervation of adjacent neurons of the same class". The Journal of Neuroscience. 16 (10): 3209–3218. doi: 10.1523/JNEUROSCI.16-10-03209.1996 . ISSN   0270-6474. PMC   6579140 . PMID   8627359.
  25. ↑ Segal, M. M. (October 1994). "Endogenous bursts underlie seizurelike activity in solitary excitatory hippocampal neurons in microcultures". Journal of Neurophysiology. 72 (4): 1874–1884. doi:10.1152/jn.1994.72.4.1874. ISSN   0022-3077. PMID   7823106.
  26. ↑ Jiang, Man; Zhu, Jie; Liu, Yaping; Yang, Mingpo; Tian, Cuiping; Jiang, Shan; Wang, Yonghong; Guo, Hui; Wang, Kaiyan (2012-05-08). "Enhancement of Asynchronous Release from Fast-Spiking Interneuron in Human and Rat Epileptic Neocortex". PLOS Biology. 10 (5): e1001324. doi: 10.1371/journal.pbio.1001324 . ISSN   1545-7885. PMC   3348166 . PMID   22589699.
  27. ↑ Nägler, Karl; Mauch, Daniela H; Pfrieger, Frank W (2001-06-15). "Glia-derived signals induce synapse formation in neurones of the rat central nervous system". The Journal of Physiology. 533 (Pt 3): 665–679. doi:10.1111/j.1469-7793.2001.00665.x. ISSN   0022-3751. PMC   2278670 . PMID   11410625.
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