Table 1.
Presynaptic long-term plasticity at excitatory and inhibitory synapses in the mammalian brain
| Brain area (species) | LTP/LTD | Synapse type | Induction protocola | Induction requirements | Referencesb |
|---|---|---|---|---|---|
| Visual cortex (rat) | LTD | Excitatory inputs, L5 pyramidal cell pairs | STDP pairing protocol | eCB signaling; postsynaptic Ca2+; presynaptic NMDAR | Sjöstrom et al. 2003; Corlew et al. 2007 |
| Immature visual cortex (mouse) | LTD | Excitatory inputs L4 to L2/3 neurons | TBS | eCB signaling; mGluR5 | Huang et al. 2008 |
| Visual cortex (mouse, rat) | LTD | GABAergic inputs to L2/3 neurons | TBS | eCB signaling; mGluR5 | Jiang et al. 2010 |
| Visual cortex (mouse) | LTP | Excitatory inputs on fast spiking GABAergic interneurons | mGluR5 (but not mGluR1), postsynaptic calcium, NMDAR-independent | Sarihi et al. 2008 | |
| Somatosensory (barrel) cortex (rat) | LTD | Excitatory inputs to L2/3 neurons | STDP pairing protocol | eCB signaling, group I mGluR; postsynaptic Ca2+; presynaptic NMDAR | Bender et al. 2006; Nevian and Sakmann 2006 |
| Sensory-motor cortex (mouse) | LTP | Excitatory inputs on somatostatin-expressing interneurons | TBS | NMDAR-independent, postsynaptic calcium-independent, PKA dependent | Chen et al. 2009 |
| Somatosensory cortex (rat) | LTP | Pyramidal cell on LTS GABAergic interneurons | STDP pairing protocol | NMDAR-dependent | Lu et al. 2007 |
| Somatosensory cortex (rat) | LTD | Pyramidal cell on LTS GABAergic interneurons | STDP pairing protocol | mGluR-dependent, NMDAR/CB1R-independent | Lu et al. 2007 |
| Prefrontal cortex (mouse) | LTD | Excitatory inputs L2/3 to L5/6 neurons | Moderate 10 Hz stimulation for 10 min | eCB signaling; postsynaptic Ca2+; mGluR5 | Lafourcade et al. 2007 |
| Prefrontal cortex (rat, mouse) | LTD | GABAergic inputs to L5/6 neuorns | Moderate 5 Hz stimulation for 5–10 min | eCB signaling; group I mGluR; presynaptic D2R | Chiu et al. 2010 |
| Thalamus (mouse) | LTP | Cortical inputs to ventrobasal neurons | (100 stim, 10 Hz) × 6 | NMDAR-independent | Castro-Alamancos and Calcagnotto 1999 |
| Hippocampus (mouse, rat, guinea pig) | LTP | Mossy fiber to CA3 pyramidal cell | HFS (25–100 Hz) | cAMP/PKA, R-type VGCC, NMDAR-independent | Harris and Cotman 1986; Zalutsky and Nicoll 1990; Huang et al. 1994; Weisskopf et al. 1994; Xiang et al. 1994; Yeckel et al. 1999 (see text for additional references) |
| Dentate (rat) | LTP | Mossy fiber to dentate gyrus basket cell | 30 Hz bursts paired with postsynaptic action potentials | PKC-dependent, PKA-independent, postsynaptic calcium | Alle et al. 2001 |
| Dentate (rat) | LTP | Mossy fiber to mossy cells | HFS (100 Hz) | NMDAR-independent | Lysetskiy et al. 2005 |
| Hippocampus (mouse, rat) | LTD | Mossy fiber to s.lucidum interneurons | HFS (100 Hz) | Postsynaptic Ca2+ via CP-AMPARs, presynaptic mGluR7, PKC | Maccaferri et al. 1998; Lei and McBain 2004; Pelkey et al. 2005, 2006 |
| Hippocampus (rat) | LTP | Mossy fiber to CA3 s.lacunosum moleculare interneurons | HFS (100 Hz) | Postsynaptic Ca2+, L-type VGCC, NMDAR-independent, postsynaptic PKA | Galvan et al. 2008, 2010 |
| Hippocampus (neonatal rat) | LTP | Immature mossy fiber to CA3 pyramidal cell | STDP pairing protocol | Postsynaptic Ca2+; L-type VGCC; NMDAR-independent; BDNF/trkB; postsynaptic cAMP/PKA | Sivakumaran et al. 2009 |
| Hippocampus (rat) | LTP | Excitatory inputs on CA1 interneurons | HFS (100 Hz), TBS | Postsynaptic Ca2+ via CP-AMPARs, NMDAR-independent | Lamsa et al. 2007; Oren et al. 2009; Nissen et al. 2010 |
| Hippocampus (rat) | LTP | Excitatory inputs on CA1 interneurons | TBS paired with postsynaptic depolarization | Postsynaptic Ca2+ and mGluR1 activation | Perez et al. 2001; Lapointe et al. 2004; Topolnik et al. 2006 |
| Hippocampus | LTD | Excitatory inputs on CA1 interneurons | HFS (100 Hz) | Retrograde signaling by 12-(S)-HPETE, presynaptic TRPV1, group I mGluR, NMDAR-independent | Gibson et al. 2008 |
| Subiculum (mouse, rat) | LTP | CA1-subiculum pyramidal cell | HFS (100 Hz) | cAMP/PKA, postsynaptic Ca2+-independent | Kokaia 2000; Wozny et al. 2008a,b |
| Hippocampus (mouse) | LTP | Schaffer collateral-CA1 pyramidal cell | HFS (200 Hz) | Postsynaptic Ca2+, L-type VGCC | Zakharenko et al. 2001; Bayazitov et al. 2007 |
| Hippocampus (mouse) | LTP | Perforant path-CA1 pyramidal cells | HFS (200 Hz) | Postsynaptic NMDARs; L-type, T-type VGCCs | Ahmed and Siegelbaum 2009 |
| Hippocampus (rat, mouse) | LTD | Inhibitory inputs to CA1 pyramidal cells | HFS, TBS | eCB signaling; group I mGluRs; cAMP/PKA; postsynaptic Ca2+ and NMDAR-independent | Chevaleyre and Castillo 2003, 2002 |
| Cerebellum (mouse, rat, guinea pig) | LTP | Parallel fiber to Purkinje cell | 4–10 Hz stimulation (e.g., 8 Hz, 30 Hz) | cAMP/PKA; NMDAR and postsynaptic Ca2+-independent | Sakurai 1987; Shibuki and Okada 1992; Salin et al. 1996b; Storm et al. 1998; Linden and Ahn 1999; Bender et al. 2009 |
| Cerebellum (mouse) | LTD | Parallel fiber to Purkinje cell | 4 Hz, in the presence of PKA inhibitor | eCB signaling NMDAR | Qiu and Knopfel 2009 |
| Cerebellum (rat) | LTP | Parallel fiber to molecular layer interneuron | 8 Hz stimulation for 30 s | cAMP/PKA | Bender et al. 2009; Rancillac and Crepel 2004 |
| Cerebellum (rat) | LTP | Parallel fiber to stellate cell | Pairing protocol: 2 Hz for 60 s, postsynaptic depolarization | cAMP-independent, NO-dependent | Rancillac and Crepel 2004 |
| Cerebellum (rat) | LTD | Parallel fiber to stellate cell | 4 × 25 stim at 30 Hz | Postsynaptic Ca2+, CP-AMPARs, mGluR1, eCB retrograde signaling, NMDAR-independent | Soler-Llavina and Sabatini 2006 |
| Cerebellum (mouse) | LTP | Stellate cell-stellate cell | HFS (100 Hz) of parallel fibers | Presynaptic NMDARs | Liu and Lachamp 2006; Lachamp et al. 2009 |
| Lateral amygdala (rat, mouse) | LTP | Cortico-lateral amygdala neurons | Simultaneous repetitive stimulation (Poisson train, 30 Hz average) of thalamic and cortical afferents | Presynaptic NMDAR, cAMP/PKA | Humeau et al. 2003; Fourcaudot et al. 2008, 2009 |
| Lateral amygdala (rat) | LTP | Cortico-lateral amygdala neurons | Pairing protocol (80 stim, 2 Hz) +30 mV postsynaptic depolarization | Postsynaptic Ca2+, NMDAR, L-type VGCC | Tsvetkov et al. 2002 |
| Lateral amygdala (rat) | LTP | Thalamic-lateral amygdala neurons | HFS (100 Hz) | Postsynaptic Ca2+, presynaptic cAMP/PKA | Huang and Kandel 1998 |
| Lateral amygdala (rat) | LTP | Thalamic-lateral amygdala neurons | PP stimulation (50 ms ISI), 2 Hz for 2 min | Presynaptic Ca2+, GluK1-containing KAR, NMDAR-independent | Shin et al. 2010 |
| Central amygdala (guinea pig) | LTP | Thalamic-central amygdala neurons | HFS (100 Hz) paired with brief suprathreshold depolarization | Presynaptic NMDAR | Samson and Pare 2005 |
| Central amygdala (rat) | LTP | Nociceptive inputs to central amygdala neurons | HFS (100 Hz) | cAMP/PKA; NMDAR-independent | Lopez de Armentia and Sah 2007 |
| Lateral amygdala (mouse) | LTD | GABAergic inputs to lateral amygdala | LFS (1 Hz) | eCB signaling; mGluR1; postsynaptic PKA activity | Marsicano et al. 2002; Azad et al. 2004 |
| Dorsal striatum (rat, mouse) | LTD | Glutamatergic cortical inputs to medium spiny neurons | HFS (100 Hz), STDP pairing protocol | eCB signaling; group I mGluR; postsynaptic Ca2+ | Gerdeman et al. 2002; Kreitzer and Malenka 2007; Shen et al. 2008 |
| Nucleus accumbens (mouse) | LTD | Glutamatergic cortical afferents to nucleus accumbens | Moderate 13 Hz stimulation for 10 min | eCB signaling; mGluR5; postsynaptic Ca2+ | Robbe et al. 2002b |
| Nucleus accumbens (mouse) | LTD | Cortical afferents to nucleus accumbens | HFS (100 Hz) | mGluR2/3, cAMP/PKA signaling | Robbe et al. 2002a |
| Ventral tegmental area (rat) | LTD | GABAergic inputs to dopamine neurons | Moderate 10 Hz stimulation for 5 min | eCB signaling; group I mGluR, D2R | Pan et al. 2008 |
| Ventral tegmental area (rat) | LTP | GABAergic inputs to dopamine neurons | HFS (100 Hz) | Postsynaptic Ca2+; NMDAR; Nitric Oxide/cGMP signaling | Nugent et al. 2007 |
| Dorsal Cochlear Nucleus (mouse) | LTD | Glutamatergic inputs to Carthwheel GABAergic interneuron | STDP paring protocol | eCB signaling; group I mGluR-indpependent | Tzounopoulos et al. 2007 |
aMost typical induction protocol is indicated. Only examples of synaptically induced (i.e., no chemically induced) LTP/LTD in brain tissue are listed.
bBecause of space limitations, not all references are listed (see text).
Abbreviations: HFS, high frequency stimulation; TBS, theta-burst stimulation; PPF, paired-pulse facilitation; CV, coefficient of variation; STDP, spike timing-dependent plasticity; VGCC, voltage-gated calcium channel, eCB, endocannabinoid; CP, Ca2+-permeable; D2R, type 2 dopamine receptor; n/a, not available.