Chapter 13 Differential mechanisms of transmission and plasticity at mossy fiber synapses

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Abstract

The last few decades have seen the hippocampal formation at front and center in the field of synaptic transmission. However, much of what we know about hippocampal short- and long-term plasticity has been obtained from research at one particular synapse; the Schaffer collateral input onto principal cells of the CA1 subfield. A number of recent studies, however, have demonstrated that there is much to be learned about target-specific mechanisms of synaptic transmission by study of the lesser known synapse made between the granule cells of the dentate gyrus; the so-called mossy fiber synapse, and its targets both within the hilar region and the CA3 hippocampus proper. Indeed investigation of this synapse has provided an embarrassment of riches concerning mechanisms of transmission associated with feedforward excitatory and inhibitory control of the CA3 hippocampus. Importantly, work from a number of labs has revealed that mossy fiber synapses possess unique properties at both the level of their anatomy and physiology, and serve as an outstanding example of a synapse designed for target-specific compartmentalization of synaptic transmission. The purpose of the present review is to highlight several aspects of this synapse as they pertain to a novel mechanism of bidirectional control of synaptic plasticity at mossy fiber synapses made onto hippocampal stratum lucidum interneurons. It is not my intention to pour over all that is known regarding the mossy fiber synapse since many have explored this topic exhaustively in the past and interested readers are directed to other fine reviews (Henze et al., 2000; Urban et al., 2001; Lawrence and McBain, 2003; Bischofberger et al., 2006; Nicoll and Schmitz, 2005).

Section snippets

Anatomy of the granule cell mossy fiber axon

Before discussing the physiological properties of the mossy fiber synapse, a short description of the granule cell anatomy and in particular the mossy fiber axon is warranted. The granule cell is the principal cell of the dentate gyrus and releases the neurotransmitter glutamate (Spruston and McBain, 2006). Granule cells typically possess small, ovoid cell bodies with a single apical, and conical dendritic tree, which extends into the molecular layer and terminates close to the hippocampal

Basic properties of mossy fiber-inhibitory interneuron transmission

Without prior electrophysiological knowledge, based on these anatomical properties alone, it is possible to speculate that the physiological properties of each synapse type within this synaptic arrangement would differ, since the large bouton alone has 20–35 release sites compared to the single release site of each filopodial extension. In fact, electrophysiological experiments have largely confirmed the hypothesis that the large and small synaptic specializations of the mossy fibers are

Two types of AMPA/NMDAR populate mossy fiber–interneuron synapses

One important aspect of mossy fiber synapses onto stratum lucidum interneurons is the nature of the AMPA and NMDA receptors that populated the postsynaptic sites. We have demonstrated that in rat hippocampus a continuum of AMPA receptor types exist at these synapses (Toth et al., 2000; Lei and McBain, 2002) (Fig. 2). Of particular interest, at one end of the continuum there are MF–interneuron synapses that comprise GluR2-lacking, Ca2+-permeable (CP-) AMPA receptors. These CP AMPA receptors lack

Mossy fiber-inhibitory interneuron plasticity

In the 1990s, Maccaferri and McBain published several papers that suggested that excitatory synapses onto inhibitory interneurons lacked the NMDAR-dependent forms of long-term potentiation (LTP) that were observed at excitatory synapses onto principal cells (Maccaferri and McBain, 1995, Maccaferri and McBain, 1996; for reviews, see McBain and Maccaferri, 1997; McBain and Maccaferri, 1997). Our failure to observe the most widely studied form of postsynaptic expressed LTP at synapses onto

mGluR7 functions as a trigger for bidirectional plasticity at the mossy fiber–interneuron synapses

The above discussion highlighted that the filopodial extensions and the parent mossy fiber bouton function independently with regard to their respective transmitter release probabilities, short-term mechanism of plasticity, and their differential sensitivity to high-frequency stimulation. This might suggest that the mechanism underlying transmitter release at each terminal is controlled by different synaptic machinery. At the large mossy fiber bouton, transmitter exocytosis is controlled by the

Implications for the mossy fiber-CA3 circuit

In most systems studied so far, it has been difficult to gauge how long-lasting plasticity at one synapse could influence activity in either the feedforward or feedback inhibitory circuit. However, our data reveal that a common induction paradigm strengthens transmission at the mossy fiber inputs onto CA3 pyramidal cells, while simultaneously weakening transmission onto stratum lucidum interneurons. These mossy fiber–interneuron synapses represent the primary feedforward inhibitory drive onto

Acknowledgment

This work was supported by an NICHD-NIH intramural award to Chris J. McBain.

References (47)

  • K.A. Pelkey et al.

    Differential regulation at functionally divergent release sites along a common axon

    Curr. Opin. Neurobiol.

    (2007)
  • K.A. Pelkey et al.

    Compartmentalized Ca2+ channel regulation at divergent mossy fiber release sites underlies target-cell dependent plasticity

    Neuron

    (2006)
  • J.I. Wadiche et al.

    Multivesicular release at climbing fiber–Purkinje cell synapses

    Neuron

    (2001)
  • H.C. Walker et al.

    Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents

    Neuron

    (2002)
  • L. Acsády et al.

    GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus

    J. Neurosci.

    (1998)
  • D.G. Amaral

    Synaptic extensions from the mossy fibers of the fascia dentate

    Anat. Embryol.

    (1979)
  • D.G. Amaral et al.

    Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions

    J. Comp. Neurol.

    (1981)
  • J. Bischofberger et al.

    Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

    Eur. J. Physiol.

    (2006)
  • A. Bragin et al.

    Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat

    J. Neurosci.

    (1995)
  • A. Bragin et al.

    Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat

    J. Neurophysiol.

    (1995)
  • P.E. Castillo et al.

    Rab3A is essential for mossy fibre long-term potentiation in the hippocampus

    Nature

    (1997)
  • P.E. Castillo et al.

    RIM1alpha is required for presynaptic long-term potentiation

    Nature

    (2002)
  • B.J. Claiborne et al.

    A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus

    J. Comp. Neurol.

    (1986)

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