Synapses are highly plastic and are modified by changes in patterns of neural activity or sensory experience. Plasticity of cortical excitatory synapses is thought to be important for learning and memory, leading to alterations in sensory representations and cognitive maps. However, these changes must be coordinated across other synapses within local circuits to preserve neural coding schemes and the organization of excitatory and inhibitory inputs, i.e., excitatory-inhibitory balance. Recent studies indicate that inhibitory synapses are also plastic and are controlled directly by a large number of neuromodulators, particularly during episodes of learning. Many modulators transiently alter excitatory-inhibitory balance by decreasing inhibition, and thus disinhibition has emerged as a major mechanism by which neuromodulation might enable long-term synaptic modifications naturally. This review examines the relationships between neuromodulation and synaptic plasticity, focusing on the induction of long-term changes that collectively enhance cortical excitatory-inhibitory balance for improving perception and behavior.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abraham WC, Bear MF. 1996. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19:126–30 [Google Scholar]
  2. Altura BM, Altura BT. 1977. Vascular smooth muscle and neurohypophyseal hormones. Fed. Proc. 36:1853–60 [Google Scholar]
  3. Artola A, Bröcher S, Singer W. 1990. Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69–72 [Google Scholar]
  4. Aston-Jones G, Cohen JD. 2005. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28:403–50 [Google Scholar]
  5. Bakin JS, Weinberger NM. 1996. The cholinergic hypothesis of geriatric memory dysfunction. PNAS 93:11219–24 [Google Scholar]
  6. Bao S, Chan VT, Merzenich MM. 2001. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412:79–83 [Google Scholar]
  7. Bartus RT, Dean RL III, Beer B, Lippa AS. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408–14 [Google Scholar]
  8. Bartz JA, Zaki J, Bolger N, Ochsner KN. 2011. Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 15:301–9 [Google Scholar]
  9. Bear MF, Singer W. 1986. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172–76 [Google Scholar]
  10. Bell CC, Han VZ, Sugawara Y, Grant K. 1997. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387:278–81 [Google Scholar]
  11. Ben-Ari Y, Woodin MA, Sernagor E, Cancedda L, Vinay L. et al. 2012. Refuting the challenges of the developmental shift of polarity of GABA actions: GABA more exciting than ever!. Front. Cell Neurosci. 6:35 [Google Scholar]
  12. Berridge CW. 2008. Noradrenergic modulation of arousal. Brain Res. Rev. 58:1–17 [Google Scholar]
  13. Bi GQ, Poo MM. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18:10464–72 [Google Scholar]
  14. 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 [Google Scholar]
  15. Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39 [Google Scholar]
  16. Bliss TVP, Lømo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:331–56 [Google Scholar]
  17. Buonomano DV, Merzenich MM. 1998. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21:149–86 [Google Scholar]
  18. Cahill L, McGaugh JL, Weinberger NM. 2001. The neurobiology of learning and memory: some reminders to remember. Trends Neurosci. 24:578–81 [Google Scholar]
  19. Carcea I, Froemke RC. 2013. Cortical plasticity, excitatory-inhibitory balance, and sensory perception. Prog. Brain Res. 207:65–90 [Google Scholar]
  20. Carter CS. 1998. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779–813 [Google Scholar]
  21. Carter ME, Yizhar O, Chikahisa S, Nguyen H, Adamantidis A. et al. 2010. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13:1526–33 [Google Scholar]
  22. Chang EF, Merzenich MM. 2003. Environmental noise retards auditory cortical development. Science 300:498–502 [Google Scholar]
  23. Christie BR, Kerr S, Abraham WC. 1994. Flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus 4:127–35 [Google Scholar]
  24. Chun S, Bayazitov IT, Blundon JA, Zakharenko SS. 2013. Thalamocortical long-term potentiation becomes gated after the early critical period in the auditory cortex. J. Neurosci. 33:7345–57 [Google Scholar]
  25. Clopath C, Busing L, Vasilaki E, Gerstner W. 2010. Connectivity reflects coding: a model of voltage-based STDP with homeostasis. Nat. Neurosci. 13:344–52 [Google Scholar]
  26. Cohen L, Rothschild G, Mizrahi A. 2011. Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72:357–69 [Google Scholar]
  27. Constantinople CM, Bruno RM. 2011. Effects and mechanisms of wakefulness on local cortical networks. Neuron 69:1061–68 [Google Scholar]
  28. D'amour JA, Froemke RC. 2015. Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex. Neuron 86514–28 [Google Scholar]
  29. Dan Y, Poo MM. 2006. Spike timing-dependent plasticity: from synapse to perception. Physiol. Rev. 86:1033–48 [Google Scholar]
  30. Debanne D, Gähwiler BH, Thompson SM. 1994. Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. PNAS 91:1148–52 [Google Scholar]
  31. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM. 2007. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J. Neurosci. 27:180–89 [Google Scholar]
  32. Dorrn AL, Yuan K, Barker AJ, Schreiner CE, Froemke RC. 2010. Developmental sensory experience balances cortical excitation and inhibition. Nature 465:932–36 [Google Scholar]
  33. Dudman JT, Tsay D, Siegelbaum SA. 2007. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 56:866–79 [Google Scholar]
  34. Dulac C, O'Connell LA, Wu Z. 2014. Neural control of maternal and paternal behaviors. Science 345:765–70 [Google Scholar]
  35. Edeline JM, Manunta Y, Hennevin E. 2011. Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation. Hear. Res. 274:75–84 [Google Scholar]
  36. Ehret G. 2005. Infant rodent ultrasounds—a gate to the understanding of sound communication. Behav. Genet. 35:19–29 [Google Scholar]
  37. Eldar E, Cohen JD, Niv Y. 2013. The effects of neural gain on attention and learning. Nat. Neurosci. 16:1146–53 [Google Scholar]
  38. Feldman DE. 2000. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex.. Neuron 27:45–56 [Google Scholar]
  39. Feldman DE. 2009. Synaptic mechanisms for plasticity in neocortex. Annu. Rev. Neurosci. 32:33–55 [Google Scholar]
  40. Feldman DE. 2012. The spike-timing dependence of plasticity. Neuron 75:556–71 [Google Scholar]
  41. Ferster D. 1986. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J. Neurosci. 6:1284–301 [Google Scholar]
  42. Fishell G, Rudy B. 2011. Mechanisms of inhibition within the telencephalon: “where the wild things are.”. Annu. Rev. Neurosci. 34:535–67 [Google Scholar]
  43. Freeman SM, Inoue K, Smith AL, Goodman MM, Young LJ. 2014. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology 45:128–41 [Google Scholar]
  44. Fritz JB, David SV, Radtke-Schuller S, Yin P, Shamma SA. 2010. Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat. Neurosci. 13:1011–19 [Google Scholar]
  45. Froemke RC, Carcea I, Barker AJ, Yuan K, Seybold BA. et al. 2013. Long-term modification of cortical synapses improves sensory perception. Nat. Neurosci. 16:79–88 [Google Scholar]
  46. Froemke RC, Dan Y. 2002. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416:433–38 [Google Scholar]
  47. Froemke RC, Debanne D, Bi GQ. 2010a. Temporal modulation of spike-timing-dependent plasticity. Front. Synaptic Neurosci. 2:19 [Google Scholar]
  48. Froemke RC, Jones BC. 2011. Development of auditory cortical synaptic receptive fields. Neurosci. Biobehav. Rev. 35:2105–13 [Google Scholar]
  49. Froemke RC, Letzkus JJ, Kampa BM, Hang GB, Stuart GJ. 2010b. Dendritic synapse location and neocortical spike-timing-dependent plasticity. Front. Synaptic Neurosci. 2:29 [Google Scholar]
  50. Froemke RC, Martins AR. 2011. Spectrotemporal dynamics of auditory cortical synaptic receptive field plasticity. Hear. Res. 279:149–61 [Google Scholar]
  51. Froemke RC, Merzenich MM, Schreiner CE. 2007. A synaptic memory trace for cortical receptive field plasticity. Nature 450:425–29 [Google Scholar]
  52. Froemke RC, Poo MM, Dan Y. 2005. Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature 434:221–25 [Google Scholar]
  53. Froemke RC, Tsay IA, Raad M, Long JD, Dan Y. 2006. Contribution of individual spikes in burst-induced long-term synaptic modification. J. Neurophysiol. 95:1620–29 [Google Scholar]
  54. Fuxe K, Borroto-Escuela DO, Romero-Fernandez W, Ciruela F, Manger P. et al. 2012. . On the role of volume transmission and receptor–receptor interactions in social behaviour: focus on central catecholamine and oxytocin neurons.. Brain Res. 1476:119–31 [Google Scholar]
  55. Gambino F, Pages S, Kehayas V, Baptista D, Tatti R. et al. 2014. Sensory-evoked LTP driven by dendritic plateau potentials in vivo. Nature 515:116–19 [Google Scholar]
  56. Gilbert CD, Li W, Piech V. 2009. Perceptual learning and adult cortical plasticity. J. Physiol. 587:2743–51 [Google Scholar]
  57. Gimpl G, Fahrenholz F. 2001. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 81:629–83 [Google Scholar]
  58. Gjorgjieva J, Clopath C, Audet J, Pfister JP. 2011. A triplet spike-timing–dependent plasticity model generalizes the Bienenstock–Cooper–Munro rule to higher-order spatiotemporal correlations. PNAS 108:19383–88 [Google Scholar]
  59. Goard M, Dan Y. 2009. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12:1444–49 [Google Scholar]
  60. Gu Q. 2002. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815–35 [Google Scholar]
  61. Gütig R, Sompolinsky H. 2006. The tempotron: a neuron that learns spike timing–based decisions. Nat. Neurosci. 9:420–28 [Google Scholar]
  62. Haas JS, Nowotny T, Abarbanel HD. 2006. Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. J. Neurophysiol. 96:3305–13 [Google Scholar]
  63. Harvey CD, Svoboda K. 2007. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450:1195–200 [Google Scholar]
  64. Harvey CD, Yasuda R, Zhong H, Svoboda K. 2008. The spread of Ras activity triggered by activation of a single dendritic spine. Science 321:136–40 [Google Scholar]
  65. Hasselmo ME. 2006. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16:710–15 [Google Scholar]
  66. Hensch TK, Fagiolini M. 2005. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 147:115–24 [Google Scholar]
  67. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A. 2008. Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature 454:1110–14 [Google Scholar]
  68. Higley MJ, Contreras D. 2006. Balanced excitation and inhibition determine spike timing during frequency adaptation. J. Neurosci. 26:448–57 [Google Scholar]
  69. Hirsch JA, Alonso JM, Reid RC, Martinez LM. 1998. Synaptic integration in striate cortical simple cells. J. Neurosci. 18:9517–28 [Google Scholar]
  70. Holmgren CD, Zilberter Y. 2001. Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells. J. Neurosci. 21:8270–77 [Google Scholar]
  71. Insanally MN, Köver H, Kim H, Bao S. 2009. Feature-dependent sensitive periods in the development of complex sound representation. J. Neurosci. 29:5456–62 [Google Scholar]
  72. Insel TR, Young LJ. 2001. The neurobiology of attachment. Nat. Rev. Neurosci. 2:129–36 [Google Scholar]
  73. Isaacson JS, Scanziani M. 2011. How inhibition shapes cortical activity. Neuron 72:231–43 [Google Scholar]
  74. Kang JI, Huppé-Gourgues F, Vaucher E. 2014. Boosting visual cortex function and plasticity with acetylcholine to enhance visual perception. Front. Syst. Neurosci. 8:172 [Google Scholar]
  75. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133–38 [Google Scholar]
  76. Kilgard MP, Merzenich MM. 1998. Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–48 [Google Scholar]
  77. Kirkwood A, Dudek SM, Gold JT, Aizenman CD, Bear MF. 1993. Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science 260:1518–21 [Google Scholar]
  78. Komatsu Y. 1994. Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J. Neurosci. 14:6488–99 [Google Scholar]
  79. Kruglikov I, Rudy B. 2008. Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58:911–24 [Google Scholar]
  80. Kuhlman SJ, Olivas ND, Tring E, Ikrar T, Xu X, Trachtenberg JT. 2013. A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501:543–46 [Google Scholar]
  81. Kullmann DM, Moreau AW, Bakiri Y, Nicholson E. 2012. Plasticity of inhibition. Neuron 75:951–62 [Google Scholar]
  82. Kuo SP, Trussell LO. 2011. Spontaneous spiking and synaptic depression underlie noradrenergic control of feed-forward inhibition. Neuron 71:306–18 [Google Scholar]
  83. Lamsa KP, Kullmann DM, Woodin MA. 2010. Spike-timing dependent plasticity in inhibitory circuits. Front. Synaptic Neurosci. 2:16 [Google Scholar]
  84. Larsen RS, Rao D, Manis PB, Philpot BD. 2010. STDP in the developing sensory neocortex. Front. Synaptic Neurosci. 2:9 [Google Scholar]
  85. Letzkus JJ, Wolff SBE, Meyer EMM, Tovote P, Courtin J. et al. 2011. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331–35 [Google Scholar]
  86. Li Y, Van Hooser SD, Mazurek M, White LE, Fitzpatrick D. 2008. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456:952–56 [Google Scholar]
  87. Lisman J, Spruston N. 2005. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat. Neurosci. 8:839–41 [Google Scholar]
  88. Liu BH, Li YT, Ma WP, Pan CJ, Zhang LI, Tao HW. 2011. Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71:542–54 [Google Scholar]
  89. Liu G. 2004. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat. Neurosci. 7:373–79 [Google Scholar]
  90. Liu RC, Schreiner CE. 2007. Auditory cortical detection and discrimination correlates with communicative significance. PLOS Biol. 5:e173 [Google Scholar]
  91. Lu JT, Li CY, Zhao JP, Poo MM, Zhang XH. 2007. Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J. Neurosci. 27:9711–20 [Google Scholar]
  92. Luhmann HJ, Prince DA. 1991. Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65:247–63 [Google Scholar]
  93. Luz Y, Shamir M. 2012. Balancing feed-forward excitation and inhibition via Hebbian inhibitory synaptic plasticity. PLOS Comput. Biol. 8:e1002334 [Google Scholar]
  94. Lynch GS, Dunwiddie T, Gribkoff V. 1977. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266:737–39 [Google Scholar]
  95. Malenka RC, Nicoll RA. 1999. Long-term potentiation: a decade of progress?. Science 285:1870–74 [Google Scholar]
  96. Manunta Y, Edeline JM. 2004. Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J. Neurophysiol. 92:1445–63 [Google Scholar]
  97. Marder E. 2012. Neuromodulation of neuronal circuits: back to the future. Neuron 76:1–11 [Google Scholar]
  98. Mariño J, Schummers J, Lyon DC, Schwabe L, Beck O. et al. 2005. Invariant computations in local cortical networks with balanced excitation and inhibition. Nat. Neurosci. 8:194–201 [Google Scholar]
  99. Markram H, Lubke J, Frotscher M, Sakmann B. 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–15 [Google Scholar]
  100. Marlin BJ, Mitre M, D'amour JA, Chao MV, Froemke RC. 2015. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520449–504 [Google Scholar]
  101. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23:649–711 [Google Scholar]
  102. Martins ARO, Froemke RC. 2014. Locus coeruleus plasticity controls cortical plasticity. Soc. Neurosci. Abstr. 363.12 [Google Scholar]
  103. McGaughy J, Everitt BJ, Robbins TW, Sarter M. 2000. The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav. Brain Res. 115:251–63 [Google Scholar]
  104. Meliza CD, Dan Y. 2006. Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49:183–89 [Google Scholar]
  105. Mesulam M. 2013. Cholinergic circuitry of the human nucleus basalis and its fate in Alzheimer's disease. J. Comp. Neurol. 521:4124–44 [Google Scholar]
  106. Metherate R, Ashe JH. 1993. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 14:132–43 [Google Scholar]
  107. Monier C, Chavane F, Baudot P, Graham LJ, Frégnac Y. 2003. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37:663–80 [Google Scholar]
  108. Montgomery N, Wehr M. 2010. Auditory cortical neurons convey maximal stimulus-specific information at their best frequency. J. Neurosci. 30:13362–66 [Google Scholar]
  109. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R. 2014. Engineering a memory with LTD and LTP. Nature 511:348–52 [Google Scholar]
  110. Nakamura T, Barbara JG, Nakamura K, Ross WN. 1999. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron 24:727–37 [Google Scholar]
  111. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K. 2000. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408:584–88 [Google Scholar]
  112. Noirot E. 1972. Ultrasounds and maternal behavior in small rodents. Dev. Psychobiol. 5:371–77 [Google Scholar]
  113. Nusser Z, Hájos N, Somogyi P, Mody I. 1998. Increased number of synaptic GABAA receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395:172–77 [Google Scholar]
  114. Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW. 2013. Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500:458–62 [Google Scholar]
  115. Owens DF, Boyce LH, Davis MBE, Kriegstein AR. 1996. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci. 16:6414–23 [Google Scholar]
  116. Pawlak V, Wickens JR, Kirkwood A, Kerr JN. 2010. Timing is not everything: Neuromodulation opens the STDP gate. Front. Synap. Neurosci. 2:146 [Google Scholar]
  117. Pawlak V, Greenberg DS, Sprekeler H, Gerstner W, Kerr JN. 2013. Changing the responses of cortical neurons from sub- to suprathreshold using single spikes in vivo. eLIFE 2:e00012 [Google Scholar]
  118. Pfister JP, Gerstner W. 2006. Triplets of spikes in a model of spike timing-dependent plasticity. J. Neurosci. 26:9673–82 [Google Scholar]
  119. Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC. et al. 2013. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16:1857–63 [Google Scholar]
  120. Pouget A, Deneve S, Ducom JC, Latham PE. 1999. Narrow versus wide tuning curves: What's best for a population code?. Neural Comput. 11:85–90 [Google Scholar]
  121. Priebe NJ, Ferster D. 2005. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133–45 [Google Scholar]
  122. Reed A, Riley J, Carraway R, Carrasco A, Perez C. et al. 2011. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70:121–31 [Google Scholar]
  123. Royer S, Paré D. 2003. Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422:518–22 [Google Scholar]
  124. Rubenstein JL, Merzenich MM. 2003. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2:255–67 [Google Scholar]
  125. Rudick CN, Gibbs RB, Woolley CS. 2003. A role for the basal forebrain cholinergic system in estrogen-induced disinhibition of hippocampal pyramidal cells. J. Neurosci. 23:4479–90 [Google Scholar]
  126. Sara SJ. 2009. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 10:211–23 [Google Scholar]
  127. Sara SJ, Segal M. 1991. Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog. Brain Res. 88:571–85 [Google Scholar]
  128. Sarter M, Parikh V, Howe WM. 2009. Phasic acetylcholine release and the volume transmission hypothesis: time to move on. Nat. Rev. Neurosci. 10:383–90 [Google Scholar]
  129. Sawchenko PE, Swanson LW. 1982. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res. Rev. 4:275–325 [Google Scholar]
  130. Scanziani M, Malenka RC, Nicoll RA. 1996. Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422:518–22 [Google Scholar]
  131. Seamans JK, Yang CR. 2004. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog. Neurobiol. 74:1–58 [Google Scholar]
  132. Seol GH, Ziburkus J, Huang S, Song L, Kim IT. et al. 2007. Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55:919–29 [Google Scholar]
  133. Sewell GD. 1970. Ultrasonic communication in rodents. Nature 227:410 [Google Scholar]
  134. Shadlen MN, Newsome WT. 1998. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18:3870–96 [Google Scholar]
  135. Shamma S, Fritz J. 2014. Adaptive auditory computations. Curr. Opin. Neurobiol. 25:164–68 [Google Scholar]
  136. Shulz DE, Sosnik R, Ego V, Haidarliu S, Ahissar E. 2000. A neuronal analogue of state-dependent learning. Nature 403:549–53 [Google Scholar]
  137. Sjöström PJ, Nelson SB. 2002. . Spike timing, calcium signals and synaptic plasticity. Curr. Opin. Neurobiol. 12:305–14 [Google Scholar]
  138. Sjöström PJ, Turrigiano GG, Nelson SB. 2001. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149–64 [Google Scholar]
  139. Sjöström PJ, Turrigiano GG, Nelson SB. 2003. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641–54 [Google Scholar]
  140. Song S, Miller KD, Abbott LF. 2000. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3:919–26 [Google Scholar]
  141. Southwell DG, Froemke RC, Alvarez-Buylla A, Stryker MP, Gandhi SP. 2010. Cortical plasticity induced by inhibitory neuron transplantation. Science 327:1145–48 [Google Scholar]
  142. Stent G. 1973. A physiological mechanism for Hebb's postulate of learning. PNAS 70:997–1001 [Google Scholar]
  143. Talwar SK, Gerstein GL. 2001. Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior. J. Neurophysiol. 86:1555–72 [Google Scholar]
  144. Talwar SK, Musial PG, Gerstein GL. 2001. Role of mammalian auditory cortex in the perception of elementary sound properties. J. Neurophysiol. 85:2350–58 [Google Scholar]
  145. Tan AYY, Atencio CA, Polley DB, Merzenich MM, Schreiner CE. 2007. Unbalanced synaptic inhibition can create intensity-tuned auditory cortex neurons. Neuroscience 146:449–62 [Google Scholar]
  146. Tan AYY, Wehr M. 2009. Balanced tone-evoked synaptic excitation and inhibition in mouse auditory cortex. Neuroscience 163:1302–15 [Google Scholar]
  147. Taub AH, Katz Y, Lampl I. 2013. Cortical balance of excitation and inhibition is regulated by the rate of synaptic activity. J. Neurosci. 33:14359–68 [Google Scholar]
  148. Thompson RF. 2005. In search of memory traces. Annu. Rev. Psychol. 56:1–23 [Google Scholar]
  149. Treue S, Maunsell JHR. 1996. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382:539–41 [Google Scholar]
  150. Turrigiano GG. 2008. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422–35 [Google Scholar]
  151. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892–96 [Google Scholar]
  152. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. 1994. . Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections.. J. Comp. Neurol. 348:351–73 [Google Scholar]
  153. Urakubo H, Honda M, Froemke RC, Kuroda S. 2008. Requirement of an allosteric kinetics of NMDA receptors for spike-timing-dependent plasticity. J. Neurosci. 28:3310–23 [Google Scholar]
  154. van Vreeswijk C, Sompolinsky H. 1996. Chaos in neural networks with balanced excitatory and inhibitory activity. Science 274:1724–26 [Google Scholar]
  155. Vogels TP, Froemke RC, Doyon N, Gilson M, Haas JS. et al. 2013. Inhibitory synaptic plasticity: spike timing-dependence and putative network function. Front. Neural Circuits 7:119 [Google Scholar]
  156. Vogels TP, Sprekeler H, Zenke F, Clopath C, Gerstner W. 2011. Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. Science 334:1569–73 [Google Scholar]
  157. Volkov IO, Galazjuk AV. 1991. Formation of spike responses to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects. Neuroscience 43:307–21 [Google Scholar]
  158. von der Malsburg C. 1973. Self-organization of orientation sensitive cells in the striate cortex. Kybernetik 14:85–100 [Google Scholar]
  159. Wang L, Maffei A. 2014. Inhibitory plasticity dictates the sign of plasticity at excitatory synapses. J. Neurosci. 34:1083–93 [Google Scholar]
  160. Wehr M, Zador AM. 2003. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–46 [Google Scholar]
  161. Wehr M, Zador AM. 2005. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47:437–45 [Google Scholar]
  162. Weinberger NM. 2007. Auditory associative memory and representational plasticity in the primary auditory cortex. Hear. Res. 229:54–68 [Google Scholar]
  163. Wittenberg GM, Wang SSH. 2006. Malleability of spike-timing-dependent plasticity at the CA3–CA1 synapse. J. Neurosci. 26:6610–17 [Google Scholar]
  164. Woodin MA, Ganguly K, Poo MM. 2003. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl transporter activity. Neuron 39:807–20 [Google Scholar]
  165. Xiong Q, Znamenskiy P, Zador AM. 2015. Selective corticostriatal plasticity during acquisition of an auditory discrimination task. Nature. In press. doi: 10.1038/nature14225 [Google Scholar]
  166. Xue M, Atallah BV, Scanziani M. 2014. Equalizing excitation-inhibition ratios across visual cortical neurons. Nature 511:596–600 [Google Scholar]
  167. Yang SN, Tang YG, Zucker RS. 1999. Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J. Neurophysiol. 81:781–87 [Google Scholar]
  168. Yao H, Shen Y, Dan Y. 2004. Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. PNAS 101:5081–86 [Google Scholar]
  169. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ. et al. 2011. Neocortical excitation/inhibition balance in information processing and social dysfunction.. Nature 477:171–78 [Google Scholar]
  170. Yu AJ, Dayan P. 2005. Uncertainty, neuromodulation, and attention. Neuron 46:681–92 [Google Scholar]
  171. Zaborszky L. 2002. The modular organization of brain systems. Basal forebrain: the last frontier. Prog. Brain Res. 136:359–72 [Google Scholar]
  172. Zhang LI, Tao HW, Holt CE, Harris WA, Poo MM. 1998. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37–44 [Google Scholar]
  173. Znamenskiy P, Zador AM. 2013. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 497:482–85 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error