Research article Special Issues

Asynchronous Segregation of Cortical Circuits and Their Function: A Life-long Role for Synaptic Death

  • Received: 13 March 2017 Accepted: 03 May 2017 Published: 09 May 2017
  • The functional role of synapse elimination has been debated since its discovery nearly three decades ago. Its widely perceived function in the removal of unnecessary and malfunctioning synapses in early life for the improvement of neural circuit performance has justified the term “synaptic pruning”. Yet, while recent experimental findings suggest the persistence of synaptic elimination into maturity and beyond, its cause and functionality have remained a mystery. Here we show that synapse elimination, caused by asynchronous neural firing, segregates individual neurons and neural circuits into interference-free synchronous isolation. Such segregation is shown to determine not only the circuit sizes, but also the circuit firing rate modes, fundamental to a large variety of cortical functions throughout life.

    Citation: Yoram Baram. Asynchronous Segregation of Cortical Circuits and Their Function: A Life-long Role for Synaptic Death[J]. AIMS Neuroscience, 2017, 4(2): 87-101. doi: 10.3934/Neuroscience.2017.2.87

    Related Papers:

  • The functional role of synapse elimination has been debated since its discovery nearly three decades ago. Its widely perceived function in the removal of unnecessary and malfunctioning synapses in early life for the improvement of neural circuit performance has justified the term “synaptic pruning”. Yet, while recent experimental findings suggest the persistence of synaptic elimination into maturity and beyond, its cause and functionality have remained a mystery. Here we show that synapse elimination, caused by asynchronous neural firing, segregates individual neurons and neural circuits into interference-free synchronous isolation. Such segregation is shown to determine not only the circuit sizes, but also the circuit firing rate modes, fundamental to a large variety of cortical functions throughout life.


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    [1] Huttenlocher PR (1979) Synaptic density in human frontal cortex. Development changes and effects of age. Brain Res 163: 195–205.
    [2] Huttenlocher PR, De Courten C, Garey LJ, et al. (1982) Synaptogenesis in human visual cortex-evidence for synapse elimination during normal development. Neurosci Lett 33: 247–252. doi: 10.1016/0304-3940(82)90379-2
    [3] Huttenlocher PR, De Courten C (1987) The development of synapses in striate cortex of man. J Neurosci 6: 1–9.
    [4] Eckenhoff MF, Rakic P (1991) A quantative analysis of synaptogenesis in the molecular layer of the dentate gyrus in the resus monkey. Develop Brain Res 64: 129–135. doi: 10.1016/0165-3806(91)90216-6
    [5] Bourgeois JP (1993) Synaptogenesis in the prefrontal cortex of the Macaque. In: B. do Boysson–Bardies (Ed.), Develop neurocog: Speech and face processing in the first year of life. Norwell, MA; Kluwer: 31–39.
    [6] Bourgeois JP, Rakic P (1993) Changing of synaptic density in the primary visual cortex of the rhesus monkey from fetal to adult age. J Neurosci 13:2801–2820.
    [7] Rakic P, Bourgeois JP, Goldman-Rakic, et al. (1994) Synaptic development of the cerebral cortex: Implications for learning, memory and mental illness. Prog in Brain Res 102: 227–243. doi: 10.1016/S0079-6123(08)60543-9
    [8] Innocenti GM (1995) Exuberant development of connections and its possible permissive role in cortical evolution. Trends Neurosci 18: 397–402. doi: 10.1016/0166-2236(95)93936-R
    [9] Takacs J, Hamori J (1994) Developmental dynamics of Purkinje cells and dendritic spines in rat cerebellar cortex. Neurosci Res 38: 515–530. doi: 10.1002/jnr.490380505
    [10] Dennis MJ, Yip JW (1978) Formation and elimination of foreign synapses on adult salamander muscle. J Physiol 274: 299–310. doi: 10.1113/jphysiol.1978.sp012148
    [11] Balice-Gordon RJ, Lichtman JW (1994) Long–term synapse loss induced by focal blockade of postsynaptlc receptors. Nature 372: 519 – 524. doi: 10.1038/372519a0
    [12] Balice-Gordon RJ, Chua C, Nelson CC, et al. (1993) Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions. Neuron 11: 801–815. doi: 10.1016/0896-6273(93)90110-D
    [13] Vanderhaeghen P, Cheng HJ (2010) Guidance Molecules in Axon Pruning and Cell death. Cold Spring Harbor Perspect in Biol 2: 1–18.
    [14] Atwood HL, Wojtowicz JM (1999) Silent Synapses in Neural Plasticity: Current Evidence. Learn Mem 6: 542–571. doi: 10.1101/lm.6.6.542
    [15] Culican SM, Nelson CC, Lichtman JW (1998) Axon withdrawal during synapse elimination at the neuromuscular junction is accompanied by disassembly of the postsynaptic specialization and withdrawal of schwann cell processes. J Neurosci 18: 4953–4965.
    [16] Chechik G, Meilijson I, Ruppin E (1998) Synaptic pruning in development: a computational account. Neur comp 10: 1759–1777. doi: 10.1162/089976698300017124
    [17] Iglesias J, Eriksson J, Grize F, et al. (2005) Dynamics of pruning in simulated large–scale spiking neural networks. BioSys 79: 11–20.
    [18] Giedd JN, Blumenthal J, Jeffries NO, et al. (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2: 861–863. doi: 10.1038/13158
    [19] Mechelli A, Crinion JT, Noppeney U, et al. (2004) Structural plasticity in the bilingual brain. Nature 431: 757. doi: 10.1038/431757a
    [20] Craik F, Bialystok E (2006) Cognition through the lifespan: mechanisms of change. Trends Cogn Sci 10: 131–138. doi: 10.1016/j.tics.2006.01.007
    [21] Lee YI, Li Y, Mikesh M, et al. (2016) Neuregulin1 displayed on motor axons regulates terminal Schwann cell–mediated synapse elimination at developing neuromuscular junctions. PNAS 113: E479–E487. doi: 10.1073/pnas.1519156113
    [22] Baram Y (2017) Developmental metaplasticity in neural circuit codes of firing and structure. Neur Net 85: 182–196. doi: 10.1016/j.neunet.2016.09.007
    [23] Lapicque L (1907) Recherches quantitatives sur l'excitation électrique des nerfs traitée comme une polarisation. J Physiol Pathol Gen 9: 620–635.
    [24] Hodgkin A, Huxley AA (1952) Quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500–544. doi: 10.1113/jphysiol.1952.sp004764
    [25] Wilson HR, Cowan JD (1972) Excitatory and Inhibitory Interactions in Localized Populations of Model Neurons. Biophys J 12: 1–24.
    [26] Abbott LF (1994) Decoding neuronal firing and modeling neural networks. Quart Rev Biophys 27: 291–331. doi: 10.1017/S0033583500003024
    [27] Gerstner W (1995)Time structure of the activity in neural network models. Phys Rev E 51: 738–758.
    [28] Baram Y (2013) Global attractor alphabet of neural firing modes. J Neurophys 110: 907–915. doi: 10.1152/jn.00107.2013
    [29] Granit RD, Kernell D, Shortess GK (1963) Quantitative aspects of repetitive firing of mammalian motoneurons caused by injected currents. J Physiol 168: 911–931. doi: 10.1113/jphysiol.1963.sp007230
    [30] Connor JA, Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21–30. doi: 10.1113/jphysiol.1971.sp009365
    [31] Carandini M, Ferster D (2000) Membrane Potential and Firing Rate in Cat Primary Visual Cortex. J Neurosci 20: 470–484.
    [32] Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2: 32–48.
    [33] Intrator N, Cooper LN (1992) Objective function formulation of the BCM theory of visual cortical plasticity: Statistical connections, stability conditions. Neur Netw 5: 3–17. doi: 10.1016/S0893-6080(05)80003-6
    [34] Cooper LN, Intrator N, Blais BS, et al. (2004) Theory of Cortical Plasticity. New Jersey: World Sciettific.
    [35] Hebb DO (1949) The organization of behavior: a neuropsychological theory. New York: Wiley.
    [36] Koenigs G (1884) Rescherches sur les integrals de certains equations fonctionnelles. Ann Sci de l'Ecole Normale Super 3: 3–41.
    [37] Lemeray EM (1895) Sur les fonctions iteratives et sur une nouvelle fonctions. Assoc Franc pour l'Advence des Sci, Congres Bordeuaux 2: 149–165.
    [38] Knoebel RA (1981) Exponential reiterated. Amer Math Month 88: 235–252. doi: 10.2307/2320546
    [39] Abraham RH, Gardini L, Mira C (1997) Chaos in Discrete Dynamical Systems. Berlin: Springer-Verlag.
    [40] Li TY, Yorke JA (1975) Period three implies chaos. Am Math Month 82: 985–992. doi: 10.2307/2318254
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