Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39 (1993).

Article  Google Scholar 

Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5–21 (2004).

Article  Google Scholar 

Markram, H., Gerstner, W. & Sjöström, P. J. Spike-timing-dependent plasticity: a comprehensive overview. Front. Synaptic Neurosci. 4, 2 (2012).

Article  Google Scholar 

Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

Article  Google Scholar 

Hensch, T. K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877–888 (2005).

Article  Google Scholar 

Cline, H. T. Topographic maps: developing roles of synaptic plasticity. Curr. Biol. 8, R836–R839 (1998).

Article  Google Scholar 

Markram, H., Gerstner, W. & Sjöström, P. J. A history of spike-timing-dependent plasticity. Front. Synaptic Neurosci. 3, 4 (2011).

Article  Google Scholar 

Hebb, D. O. The Organization of Behaviour (Wiley, 1949).

Shatz, C. J. The developing brain. Sci. Am. 267, 60–67 (1992).

Article  Google Scholar 

Löwel, S. & Singer, W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255, 209–212 (1992).

Article  Google Scholar 

Hebb, D. O. A Textbook of Psychology (W. B. Saunders, 1972).

Hopfield, J. J. & Tank, D. W. Computing with neural circuits: a model. Science 233, 625–633 (1986).

Article  Google Scholar 

McBain, C. J., Freund, T. F. & Mody, I. Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci. 22, 228–235 (1999).

Article  Google Scholar 

Sjöström, P. J., Rancz, E. A., Roth, A. & Häusser, M. Dendritic excitability and synaptic plasticity. Physiol. Rev. 88, 769–840 (2008).

Article  Google Scholar 

Maheux, J., Froemke, R. C. & Sjöström, P. J. in Dendrites Ch. 18 (eds Stuart, G., Spruston, N. & Häusser, M.) 465–498 (Oxford Univ. Press, 2016).

Yazaki-Sugiyama, Y., Kang, S., Cateau, H., Fukai, T. & Hensch, T. K. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 462, 218–221 (2009). In this work, in vivo visual cortex recordings following monocular deprivation reveal that BCs have an unexpected initial preference for the occluded eye before a late preference for the open eye, in keeping with temporally symmetric STDP at excitatory inputs to BCs.

Article  Google Scholar 

Udakis, M., Pedrosa, V., Chamberlain, S. E. L., Clopath, C. & Mellor, J. R. Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output. Nat. Commun. 11, 4395 (2020). Using computer modelling, this study demonstrates that timing-dependent LTP at SST+IN inputs onto CA1 PCs stabilizes hippocampal place cells and prevents interference in new environments, whereas timing-dependent LTD at PV+IN inputs maintains place cell spike output.

Article  Google Scholar 

Vogels, T. P., Sprekeler, H., Zenke, F., Clopath, C. & Gerstner, W. Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. Science 334, 1569–1573 (2011).

Article  Google Scholar 

Kullmann, D. M. & Lamsa, K. P. LTP and LTD in cortical GABAergic interneurons: emerging rules and roles. Neuropharmacology 60, 712–719 (2011).

Article  Google Scholar 

Lamsa, K. P., Heeroma, J. H., Somogyi, P., Rusakov, D. A. & Kullmann, D. M. Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315, 1262–1266 (2007).

Article  Google Scholar 

Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793–807 (2004).

Article  Google Scholar 

Ascoli, G. A. et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557–568 (2008).

Article  Google Scholar 

Gouwens, N. W. et al. Integrated morphoelectric and transcriptomic classification of cortical GABAergic cells. Cell 183, 935–953.e19 (2020).

Article  Google Scholar 

Larsen, R. S. & Sjöström, P. J. Synapse-type-specific plasticity in local circuits. CONB 35, 127–135 (2015). This review defines the research field of synapse type-specific plasticity in local circuits.

Google Scholar 

Sjöström, P. J. Grand challenge at the frontiers of synaptic neuroscience. Front. Synaptic Neurosci. 13, 748937 (2021).

Article  Google Scholar 

Abbott, L. F. et al. The mind of a mouse. Cell 182, 1372–1376 (2020).

Article  Google Scholar 

Gregory, S. G. et al. A physical map of the mouse genome. Nature 418, 743–750 (2002).

Article  Google Scholar 

Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014).

Article  Google Scholar 

Rudy, B., Fishell, G., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).

Article  Google Scholar 

Tremblay, R., Lee, S. & Rudy, B. GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron 91, 260–292 (2016).

Article  Google Scholar 

Pfeffer, C. K., Xue, M., He, M., Huang, Z. J. & Scanziani, M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068–1076 (2013).

Article  Google Scholar 

Kawaguchi, Y. & Kubota, Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70, 387–396 (1993).

Article  Google Scholar 

Mele, M., Leal, G. & Duarte, C. B. Role of GABAA R trafficking in the plasticity of inhibitory synapses. J. Neurochem. 139, 997–1018 (2016).

Article  Google Scholar 

Kullmann, D. M., Moreau, A. W., Bakiri, Y. & Nicholson, E. Plasticity of inhibition. Neuron 75, 951–962 (2012).

Article  Google Scholar 

Chiu, C. Q., Barberis, A. & Higley, M. J. Preserving the balance: diverse forms of long-term GABAergic synaptic plasticity. Nat. Rev. Neurosci. 20, 272–281 (2019).

Article  Google Scholar 

Capogna, M., Castillo, P. E. & Maffei, A. The ins and outs of inhibitory synaptic plasticity: neuron types, molecular mechanisms and functional roles. Eur. J. Neurosci. 54, 6882–6901 (2021).

Article  Google Scholar 

Wu, Y. K., Miehl, C. & Gjorgjieva, J. Regulation of circuit organization and function through inhibitory synaptic plasticity. Trends Neurosci. https://doi.org/10.1016/j.tins.2022.10.006 (2022).

Article  Google Scholar 

Sprekeler, H. Functional consequences of inhibitory plasticity: homeostasis, the excitation–inhibition balance and beyond. Curr. Opin. Neurobiol. 43, 198–203 (2017).

Article  Google Scholar 

Topolnik, L. & Tamboli, S. The role of inhibitory circuits in hippocampal memory processing. Nat. Rev. Neurosci. https://doi.org/10.1038/s41583-022-00599-0 (2022).

Article  Google Scholar 

Hensch, T. K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508 (1998).

Article  Google Scholar 

Maffei, A., Nataraj, K., Nelson, S. B. & Turrigiano, G. G. Potentiation of cortical inhibition by visual deprivation. Nature 443, 81–84 (2006). This work shows that visual deprivation leaves excitatory connections in L4 unaffected but potentiates BC inhibition of PCs, which shifts the E/I balance in PCs to favour inhibition and may, thus, underlie deprivation-induced degradation of visual function.

Article  Google Scholar 

Sjöström, P. J. & Gerstner, W. Spike-timing dependent plasticity. Scholarpedia 5, 1362 (2010).

Article  Google Scholar 

Song, S., Miller, K. D. & Abbott, L. F. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3, 919–926 (2000).

Article  Google Scholar 

Vickers, E. D. et al. Parvalbumin-interneuron output synapses show spike-timing-dependent plasticity that contributes to auditory map remodeling. Neuron 99, 720–735.e6 (2018). Using paired recordings in L4 of auditory cortex, this work shows how critical period sound exposure transforms the sign of plasticity from LTD to LTP at PV+IN to PC synapses, which may provide disinhibition during critical period plasticity.

Article  Google Scholar 

Field, R. E. et al. Heterosynaptic plasticity determines the set point for cortical excitatory–inhibitory balance. Neuron https://doi.org/10.1016/j.neuron.2020.03.002 (2020). Using electrode stimulation arrays, this work finds that, in developing auditory cortex, homosynaptic and heterosynaptic excitatory and inhibitory inputs to L5 PCs all exhibit STDP; however, compared with homosynaptic inputs, heterosynaptic inputs have a stronger influence on the set point for overall E/I balance.

Article  Google Scholar 

Wang, L. & Maffei, A. Inhibitory plasticity dictates the sign of plasticity at excitatory synapses. J. Neurosci. 34, 1083–1093 (2014).

Article  Google Scholar 

D’Amour, J. A. & Froemke, R. C. Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex. Neuron https://doi.org/10.1016/j.neuron.2015.03.014 (2015). This work shows how both inhibitory and excitatory neocortical synapses are modified by STDP and how inhibitory plasticity depends on the initial E/I ratio, which helps maintain E/I balance.

Article  Google Scholar 

Lourenço, J. et al. Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons. PLoS Biol. 12, e1001903 (2014). This work shows that, in L5 PCs, the selective potentiation of perisomatic inhibition via nitric oxide retrograde signalling alters the ability to integrate excitatory inputs and improves spiking precision.

Article  Google Scholar 

Wiesel, T. N. & Hubel, D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).

Article  Google Scholar 

Kuhlman, S. J. et al. A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501, 543–546 (2013).

Article  Google Scholar 

Lu, J. T., Li, C. Y., Zhao, J. P., Poo, M. M. & Zhang, X. H. Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J. Neurosci. 27, 9711–9720 (2007). This work shows that PC–MC synapses exhibit the classical temporally asymmetric STDP also found at PC–PC connections, although plasticity at these two synapse types relies on different mechanisms, whereas PC–BC synapses connections depress irrespective of relative timing.

Article  Google Scholar 

Xue, M., Atallah, B. V. & Scanziani, M. Equalizing excitation–inhibition ratios across visual cortical neurons. Nature 511, 596–600 (2014).

Article  Google Scholar 

Hennequin, G., Agnes, E. J. & Vogels, T. P. Inhibitory plasticity: balance, control, and codependence. Annu. Rev. Neurosci. 40, 557–579 (2017).

Article  Google Scholar 

Blackman, A. V., Abrahamsson, T., Costa, R. P., Lalanne, T. & Sjöström, P. J. Target cell-specific short-term plasticity in local circuits. Front. Synaptic Neurosci. 5, 1–13 (2013).

Article  Google Scholar 

Costa, R. P., Froemke, R. C., Sjöström, P. J. & van Rossum, M. C. W. Unified pre- and postsynaptic long-term plasticity enables reliable and flexible learning. eLife https://doi.org/10.7554/eLife.09457 (2015).