Talking back: dendritic neurotransmitter release

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Abstract

Classical transmitters and neuropeptides can be released from the dendrites of many neuronal populations, to act as retrograde signals that modulate synaptic transmission, electrical activity and, in some cases, morphology of the cell of origin. For the hypothalamic neuroendocrine cells that release vasopressin and oxytocin, the stimuli, mechanisms and physiological functions of dendritic release have been revealed in detail that is not yet available for other neurons. The regulation of dendritic transmitter release is complex and at least partially independent from axon terminal release. Here, we provide an overview of recent findings on the mechanisms and physiological consequences of dendritic neuropeptide release and place this in the context of discoveries of dendritic neurotransmitter release in other brain regions.

Section snippets

Classical transmitters

It is now clear that ‘classical transmitters’ are also major players in retrograde signalling. The many sites within the CNS at which dendritic signalling has been reported to occur are depicted in Fig. 1. Dopamine 4, 5 and ATP [6] were among the first neuroactive substances shown to be released from dendrites. Activation of ionotropic NMDA receptors in the substantia nigra triggers Ca2+-dependent dendritic release of dopamine [7] and these neurons are endowed with dopamine D2 and D3

Neuropeptides – vasopressin and oxytocin

Among the best-established sites of dendritic release are the hypothalamic supraoptic nucleus (SON) and paraventricular (PVN) nuclei (Fig. 1, Fig. 2), where the magnocellular neurons (MCNs) release the peptides vasopressin and oxytocin from their somato–dendritic compartment (Fig. 2a). Studies on dendritic release from these neurons have been facilitated by the fact that their somata and dendrites are tightly grouped, making it possible to measure the dynamics of release using microdialysis

Mechanisms of dendritic release

Differential release of neurotransmitters from different compartments of a single neuron requires subtle regulatory mechanisms. Here, we present what is known about dendritic release mechanisms and contrast this with our understanding of parallel processes in the axon terminals.

Development and morphological plasticity

During development, vasopressin- and oxytocin-containing cells maintain spontaneous electrical activity via depolarization and a facilitation of their own dendritic release. This autocontrol loop is maximally active during the second postnatal week, correlating with a transient increase in dendritic branching. Dendritic branching requires interplay between release of peptides from dendrites and glutamate from presynaptic terminals 42, 50.

In the adult animal, the somata, dendrites and axon

Concluding remarks

For many years the phenomenon of dendritic transmitter release was thought to be a peculiarity of the dopaminergic neurons of the substantia nigra. With the evidence that gaseous transmitters act as signalling molecules to mediate plasticity of synaptic function during LTP, the idea of retrograde transmission gained wider credence. Here, we present evidence that retrograde synaptic communication is also a feature of the neuropeptides, which comprise the largest group of transmitters in the

Acknowledgements

This work was supported by grants from the Wellcome Trust, BBSRC (M.L.) and Canadian Institutes of Health Research (Q.J.P.). Quentin Pittman is an Alberta Heritage Foundation for Medical Research Medical Scientist. Thanks to our many colleagues who reviewed and provided constructive advice on this paper.

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