5439
J Physiol 594.19 (2016) pp 5439–5440
The Journal of Physiology
Neuroscience
EDITORIAL
Synaptic signalling and plasticity: emerging new players ´ Katalin Toth Quebec Mental Health Institute, Department of Psychiatry and Neuroscience, Universit´e Laval, Quebec City, Quebec, Canada Email: [email protected]
Interactions between neurons and networks continuously change in order to adapt to relevant tasks and allow proper behavioural responses; these changes can be short-lived or enduring and strongly rely on functional rearrangement at the level of individual synapses. In the decades following the discovery of long-term potentiation by Bliss & Lomo (1973), various key elements of structural and functional synaptic modification leading to altered synaptic strength have been unveiled. These include the demonstration of activation of NMDA receptors (Collingridge et al. 1983), their activation at the synapse (Forsythe & Westbrook, 1988), calcium permeability and rise in postsynaptic calcium (Lynch et al. 1983; MacDermott et al. 1986), with the resultant insertion of postsynaptic receptors (Isaac et al. 1995; Liao et al. 1995) and increase in presynaptic release probability (Zalutsky & Nicoll, 1990). On a shorter time scale, changes occurring in the millisecond and second range have been shown to play a pivotal role in information processing and transfer (Zucker & Regehr, 2002). In recent years, this initial picture has gained substantial depth with the discovery of various auxiliary proteins (Jackson & Nicoll, 2011) and the emergence of increasingly complex celland synapse-specific signalling patterns. How do structural and functional changes endow the synapse and the network with the necessary flexibility to adapt to ever changing input patterns? What are the pathological consequences of dysfunctional synaptic plastic changes and network development? Current advances presented at the 5th European Synapse Meeting held in Bristol on 7–9 September 2015 highlighted the importance of newly emerging regulatory processes in synaptic signalling and plasticity. This meeting and
the reviews presented here provide new insights into the complexity and subtlety of synaptic signalling and plasticity. In the current issue, a review by Ivanova et al. (2016) investigates the role of two key members of the complex at the presynaptic active zone in short- and long-term changes in synaptic signalling. They underline the complex nature of presynaptic regulatory mechanisms that can act via posttranslational modification and presynapse-to-nucleus retrograde signalling. These vastly distinct functions influence neuronal signalling for a very short period (seconds) or work on a slower time scale via the reconfiguration of gene expression. Garc´ıa-Nafr´ıa et al. (2016) detail new advances in the dynamic regulation of AMPA receptor function via modifications in the extracellular region that is composed of ligand-binding pocket and amino-terminal compartments. These regions can go through significant conformational changes and regulate interaction with myriad proteins in the synapse. The review explores the potential interaction between the reconfiguration of the extracellular region and preand postsynaptic interacting proteins that could alter synaptic signalling and plasticity. Recent studies shed light in the importance of DISC1 in the development of schizophrenia. A review by Devine et al. (2016) highlights research suggesting that DISC1 is chiefly responsible for the regulation of intracellular trafficking. DISC1 can influence the trafficking of a wide range of cargo from mRNA to neurotransmitter receptors. This latter could potentially explain dysfunctional DISC1’s role in impaired synaptic plasticity. During the development of functioning networks, the timely insertion of receptors with a particular subunit composition plays a critical role. The ‘fingerprints’ of glutamate receptor subunits in various subpopulations of interneurons can be predicted from their embryonic origins. The review by Akg¨ul & McBain (2016) highlights recent developments regarding the roles different types of iGluRs play in the development of inhibitory networks.
C 2016 The Authors. The Journal of Physiology C 2016 The Physiological Society
The developmental iGluR profiles of interneurons derived from the medial ganglionic eminence and caudal ganglionic eminence, as well as the role they pay in the maturation of the circuit, could significantly influence network function. References Akg¨ul G & McBain CJ (2016). Diverse roles for ionotropic glutamate receptors on inhibitory interneurons in developing and adult brain. J Physiol 594, 5471–5490. Bliss TV & Lomo 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, 331–356. Collingridge GL, Kehl SJ & McLennan H (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334, 33–46. Devine MJ, Norkett R & Kittler KT (2016). DISC1 is a coordinator of intracellular trafficking to shape neuronal development and connectivity. J Physiol 594, 5459–5469. Forsythe ID & Westbrook GL (1988). Slow excitatory postsynaptic currents mediated by N-methyl-D-aspartate receptors on cultured mouse central neurons. J Physiol 396, 515–533. Garc´ıa-Nafr´ıa J, Herguedas B, Watson JF & Greger IH (2016). The dynamic AMPA receptor extracellular region: a platform for synaptic protein interactions. J Physiol 594, 5449–5458. Isaac JTR, Nicoll RA & Malenka RC (1995). Evidence for silent synapses. Implications for the expression of LTP. Neuron 15, 427−434. Ivanova D, Dirks A & Fejtova A (2016). Bassoon and piccolo regulate ubiquitination and link presynaptic molecular dynamics with activity-regulated gene expression. J Physiol 594, 5441–5448. Jackson AC & Nicoll RA (2011). The expanding social network of ionotropic glutamate receptors: TARPS and other transmembrane auxiliary subunits. Neuron 70, 178–199. Liao DZ, Hessler NA & Malinow R (1995). Activation of postsynaptically silent synapses during pairing induced LTP in CA1 region of hippocampal slice. Nature 375, 400–404. Lynch G, Larson J, Kelso S, Barrionuevo G & Schottler F (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719–721.
DOI: 10.1113/JP272719
5440 MacDermott AB, Mayer ML, Westbrook GL, Smith SJ & Barker JL (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519–522.
Editorial Zalutsky RA & Nicoll RA (1990). Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248, 1619–1624.
J Physiol 594.19
Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355–405. Additional information Competing interests
None.
C 2016 The Authors. The Journal of Physiology C 2016 The Physiological Society
J Physiol 594.19 (2016) pp 5439–5440
The Journal of Physiology
Neuroscience
EDITORIAL
Synaptic signalling and plasticity: emerging new players ´ Katalin Toth Quebec Mental Health Institute, Department of Psychiatry and Neuroscience, Universit´e Laval, Quebec City, Quebec, Canada Email: [email protected]
Interactions between neurons and networks continuously change in order to adapt to relevant tasks and allow proper behavioural responses; these changes can be short-lived or enduring and strongly rely on functional rearrangement at the level of individual synapses. In the decades following the discovery of long-term potentiation by Bliss & Lomo (1973), various key elements of structural and functional synaptic modification leading to altered synaptic strength have been unveiled. These include the demonstration of activation of NMDA receptors (Collingridge et al. 1983), their activation at the synapse (Forsythe & Westbrook, 1988), calcium permeability and rise in postsynaptic calcium (Lynch et al. 1983; MacDermott et al. 1986), with the resultant insertion of postsynaptic receptors (Isaac et al. 1995; Liao et al. 1995) and increase in presynaptic release probability (Zalutsky & Nicoll, 1990). On a shorter time scale, changes occurring in the millisecond and second range have been shown to play a pivotal role in information processing and transfer (Zucker & Regehr, 2002). In recent years, this initial picture has gained substantial depth with the discovery of various auxiliary proteins (Jackson & Nicoll, 2011) and the emergence of increasingly complex celland synapse-specific signalling patterns. How do structural and functional changes endow the synapse and the network with the necessary flexibility to adapt to ever changing input patterns? What are the pathological consequences of dysfunctional synaptic plastic changes and network development? Current advances presented at the 5th European Synapse Meeting held in Bristol on 7–9 September 2015 highlighted the importance of newly emerging regulatory processes in synaptic signalling and plasticity. This meeting and
the reviews presented here provide new insights into the complexity and subtlety of synaptic signalling and plasticity. In the current issue, a review by Ivanova et al. (2016) investigates the role of two key members of the complex at the presynaptic active zone in short- and long-term changes in synaptic signalling. They underline the complex nature of presynaptic regulatory mechanisms that can act via posttranslational modification and presynapse-to-nucleus retrograde signalling. These vastly distinct functions influence neuronal signalling for a very short period (seconds) or work on a slower time scale via the reconfiguration of gene expression. Garc´ıa-Nafr´ıa et al. (2016) detail new advances in the dynamic regulation of AMPA receptor function via modifications in the extracellular region that is composed of ligand-binding pocket and amino-terminal compartments. These regions can go through significant conformational changes and regulate interaction with myriad proteins in the synapse. The review explores the potential interaction between the reconfiguration of the extracellular region and preand postsynaptic interacting proteins that could alter synaptic signalling and plasticity. Recent studies shed light in the importance of DISC1 in the development of schizophrenia. A review by Devine et al. (2016) highlights research suggesting that DISC1 is chiefly responsible for the regulation of intracellular trafficking. DISC1 can influence the trafficking of a wide range of cargo from mRNA to neurotransmitter receptors. This latter could potentially explain dysfunctional DISC1’s role in impaired synaptic plasticity. During the development of functioning networks, the timely insertion of receptors with a particular subunit composition plays a critical role. The ‘fingerprints’ of glutamate receptor subunits in various subpopulations of interneurons can be predicted from their embryonic origins. The review by Akg¨ul & McBain (2016) highlights recent developments regarding the roles different types of iGluRs play in the development of inhibitory networks.
C 2016 The Authors. The Journal of Physiology C 2016 The Physiological Society
The developmental iGluR profiles of interneurons derived from the medial ganglionic eminence and caudal ganglionic eminence, as well as the role they pay in the maturation of the circuit, could significantly influence network function. References Akg¨ul G & McBain CJ (2016). Diverse roles for ionotropic glutamate receptors on inhibitory interneurons in developing and adult brain. J Physiol 594, 5471–5490. Bliss TV & Lomo 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, 331–356. Collingridge GL, Kehl SJ & McLennan H (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334, 33–46. Devine MJ, Norkett R & Kittler KT (2016). DISC1 is a coordinator of intracellular trafficking to shape neuronal development and connectivity. J Physiol 594, 5459–5469. Forsythe ID & Westbrook GL (1988). Slow excitatory postsynaptic currents mediated by N-methyl-D-aspartate receptors on cultured mouse central neurons. J Physiol 396, 515–533. Garc´ıa-Nafr´ıa J, Herguedas B, Watson JF & Greger IH (2016). The dynamic AMPA receptor extracellular region: a platform for synaptic protein interactions. J Physiol 594, 5449–5458. Isaac JTR, Nicoll RA & Malenka RC (1995). Evidence for silent synapses. Implications for the expression of LTP. Neuron 15, 427−434. Ivanova D, Dirks A & Fejtova A (2016). Bassoon and piccolo regulate ubiquitination and link presynaptic molecular dynamics with activity-regulated gene expression. J Physiol 594, 5441–5448. Jackson AC & Nicoll RA (2011). The expanding social network of ionotropic glutamate receptors: TARPS and other transmembrane auxiliary subunits. Neuron 70, 178–199. Liao DZ, Hessler NA & Malinow R (1995). Activation of postsynaptically silent synapses during pairing induced LTP in CA1 region of hippocampal slice. Nature 375, 400–404. Lynch G, Larson J, Kelso S, Barrionuevo G & Schottler F (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719–721.
DOI: 10.1113/JP272719
5440 MacDermott AB, Mayer ML, Westbrook GL, Smith SJ & Barker JL (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519–522.
Editorial Zalutsky RA & Nicoll RA (1990). Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248, 1619–1624.
J Physiol 594.19
Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355–405. Additional information Competing interests
None.
C 2016 The Authors. The Journal of Physiology C 2016 The Physiological Society
