The Grass Roots of Synapse Suppression

نویسندگان

  • Johanna M. Montgomery
  • Daniel V. Madison
چکیده

actual trigger for DSI appears to be a rise in postsynaptic calcium, since it is prevented when calcium chelators, such as EGTA or BAPTA, are present postJohanna M. Montgomery and Daniel V. Madison* Department of Molecular and Cellular Physiology Stanford University School of Medicine synaptically (Llano et al., 1991; Pitler and Alger, 1994). Stanford, California 94305 Following induction, DSI can last for up to 2 min. Because the synapses suppressed are inhibitory, DSI moves the postsynaptic cell into a transient state of Not counting recreational use, the effects of marijuana heightened excitability. Such an alteration in cell exciton the brain have been under active investigation for at ability could decrease the threshold for action potential least the past 30 years. Important milestones in the firing and may serve to selectively enhance excitatory elucidation of the physiological actions of psychoactive inputs following depolarization. Decreases in inhibition substances from cannabis sativa included the discovery have been shown to facilitate both NMDA receptor–mediof neuronal receptor proteins for cannabinoids and the ated excitatory currents and the subsequent induction of existence of endogenous cannabinoid substances (SulNMDAR-dependent changes in synaptic strength. livan, 2000). In this issue of Neuron, two papers appear Though the induction of DSI is postsynaptic, its ex(Kreitzer and Regehr, 2001; Ohno-Shosaku et al., 2001), pression appears to be a presynaptic phenomenon as which along with another in Nature (Wilson and Nicoll, suggested by a lack of change in both quantal size and 2001), provide new and important insight into the dein postsynaptic cell sensitivity to iontophoresed GABA tailed mechanisms by which endogenous cannabinoids (Pitler and Alger, 1992; Alger et al., 1996). This implies exert their effects on nervous physiology. These papers that, in the production of DSI, information is moving report that endogenous cannabinoids released from backward across the synapse, from postsynaptic inducpostsynaptic neurons after depolarization act on pretion to presynaptic expression, and thus that a retrosynaptic terminals to suppress subsequent neurotransgrade message originates in the postsynaptic cell and mitter release, driving the synapse into an altered state. acts presynaptically to depress presynaptic function The broad behavioral effects of cannabinoid intoxica(Llano et al., 1991). Hypotheses concerning the identity tion such as impaired learning and memory, depressed of the messenger carrying this retrograde signal have cognitive skills, decreased motor coordination, and alcentered on glutamate or a glutamate-like substance terations in pain perception and emotional state, likely released from the postsynaptic cell through vesicular reflect its widespread action in many brain regions. Infusion and acting through presynaptic metabotropic gludeed, cannabinoid receptors are highly expressed tamate receptors (mGluR) (Glitsch et al., 1996; Morishita throughout the central nervous system (Sullivan, 2000). et al., 1998). In the cerebellum, a selective group II CB1, a G protein–linked cannabinoid receptor, is exmGluR agonist was shown to occlude DSI expression, pressed on the presynaptic terminals of inhibitory inand DSI was reduced (although not blocked) in the presterneurons in the hippocampus and on presynaptic parence of L-AP3, a group I mGluR antagonist. Curiously, allel and climbing fibers throughout the molecular layer however, the broad-spectrum inhibitor MCPG had no in the cerebellum. To date, two endogenous cannabieffect on DSI. Similarly, in the hippocampus the mGluR noids have been isolated, the phospholipid derivatives agonist ACPD decreased GABAA IPSCs and suppressed anandamide and sn-2 arachidonylglycerol (2-AG) (DeDSI by z50%. DSI was proposed to be expressed by vane et al., 1992; Stella et al., 1997). While there is no glutamate acting on type I mGluRs as the use of group doubt that many of their physiological roles still await I agonists occluded DSI. Again, however, even very high discovery, endogenous cannabinoids are known to have concentrations of MCPG failed to completely block DSI significant effects on synaptic physiology. Specifically, expression (Morishita et al., 1998). Now, three new papers have appeared that bring the 2-AG depresses release of the transmitters glutamate, field to a new high. Two papers appearing in this issue g-amino butyric acid (GABA), and acetylcholine in the of Neuron and one in Nature have provided significant hippocampus (Sullivan, 2000). Many downstream efinsight into the mechanisms of depolarization-induced fects likely result from such an action, one of which synapse suppression and have identified the retrograde is that a decrease in glutamate release decreases the messenger as being an endogenous cannabinoid (Figeffectiveness of stimuli in the induction of long-term ure 1). In addition, they contain evidence against a role potentiation and long-term depression (Lévénès et al., for glutamate in this retrograde transmission as all three 1998; Misner and Sullivan, 1999), two forms of synaptic of these studies fail to show an effect of mGluR antagoplasticity thought to be involved in learning and memory. nists on depolarization-induced suppression. PostsynSome GABAergic inhibitory synapses display an interaptically applied botulinum toxin, which blocks vesicle esting property known as depolarization-induced supfusion, does not inhibit DSI (Wilson and Nicoll, 2001), pression of inhibition, or DSI, during which their function making vesicular glutamate release from the postsynapis suppressed following depolarization of the postsyntic cell highly improbable. While synapse suppression aptic cell (Llano et al., 1991; Alger and Pitler, 1995). The is normally induced by postsynaptic depolarization, it is not absolutely required, as postsynaptic liberation of calcium alone, via flash photolysis of caged calcium, * To whom correspondence should be addressed (e-mail: madison@

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عنوان ژورنال:
  • Neuron

دوره 29  شماره 

صفحات  -

تاریخ انتشار 2001