The emergence of the volume transmission concept 1 Published on the World Wide Web on 12 January 1998. 1

Interneuronal communication in the central nervous system (CNS) have always been of basic importance for theories on the cerebral morphofunctional architecture. Our group has proposed that intercellular communication in the brain can be grouped into 2 broad classes based on some general features of the transmission: wiring (WT) and volume (VT) transmission. WT occurs via a relatively constrained cellular chain (wire), while VT consists of 3-dimensional diffusion of signals in the extracellular fluid (ECF) for distances larger than the synaptic cleft. Both morphological and functional evidence indicates that dopamine (DA) synapses in striatum are 'open' synapses, i.e., synapses which favor diffusion of the transmitter into the surrounding ECF and observations are compatible with the view that DA varicosities can synthesize, store and release DA for VT. The DAergic mesostriatal transmission has, therefore, been examined by several groups to give experimental support to VT. Moreover, due to its minor structural requirements, VT may become prevalent under some pathological conditions, e. g. Parkinson's disease. In animal models of DAergic pathway degeneration, it has been shown that a compensatory activation of surviving DA terminals may lead to a preferential potentiation of VT. WT and VT favor different and complementary types of computation. VT is markedly slower and less safe than WT, but has minor spatial constraints and allows the reach of a large number of targets. Models of neuronal systems integrating classical neuronal circuits and diffusible signals begin to show how WT and VT may interact in the neural tissue.

[1]  G. Snyder,et al.  Dopamine efflux from striatal slices after intracerebral 6-hydroxydopamine: evidence for compensatory hyperactivity of residual terminals. , 1990, The Journal of pharmacology and experimental therapeutics.

[2]  P. Garris,et al.  Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  K. Fuxe,et al.  Evidence for volume transmission in the dopamine denervated neostriatum of the rat after a unilateral nigral 6-OHDA microinjection. Studies with systemic d-amphetamine treatment , 1994, Brain Research.

[4]  F. Gonon Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry , 1988, Neuroscience.

[5]  T. Sejnowski,et al.  The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms. , 1994, Learning & memory.

[6]  B. Bunney,et al.  Activity of A9 and A10 dopaminergic neurons in unrestrained rats: further characterization and effects of apomorphine and cholecystokinin , 1987, Brain Research.

[7]  M. Herkenham,et al.  Mismatches between neurotransmitter and receptor localizations in brain: observations and implications , 1987, Neuroscience.

[8]  Luigi F. Agnati,et al.  Wiring and volume transmission in the central nervous system: The concept of closed and open synapses , 1996, Progress in Neurobiology.

[9]  L. Descarries,et al.  Ultrastructural basis of monoamine and acetylcholine function in CNS , 1995 .

[10]  H. Schaible,et al.  Calcitonin Gene‐related Peptide Causes Intraspinal Spreading of Substance P Released by Peripheral Stimulation , 1992, The European journal of neuroscience.

[11]  C. Jahr,et al.  Transporters Buffer Synaptically Released Glutamate on a Submillisecond Time Scale , 1997, The Journal of Neuroscience.

[12]  M. Kuhar The mismatch problem in receptor mapping studies , 1985, Trends in Neurosciences.

[13]  Luigi F. Agnati,et al.  Volume transmission in the brain. Novel mechanisms for neural transmission Edited by K. Fuxe and L.F. Agnati, Advances in neuroscience vol. 1, Raven Press, New York, 1991, 602 pp., US$ 130,- , 1992, Neuroscience Letters.

[14]  Y. Agid,et al.  DA Uptake Sites, D1, and D2 Receptors, D2 and Preproenkephalin mRNAs and Fos Immunoreactivity in Rat Striatal Subregions after Partial Dopaminergic Degeneration , 1996, The European journal of neuroscience.

[15]  D. Madison,et al.  Locally distributed synaptic potentiation in the hippocampus. , 1994, Science.

[16]  S. Sesack,et al.  Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  K. Murphy,et al.  The suppression of long-term potentiation in rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent , 1993, Neuron.

[18]  T. Dawson,et al.  Gases as biological messengers: nitric oxide and carbon monoxide in the brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  C. Nicholson,et al.  Hindered diffusion of high molecular weight compounds in brain extracellular microenvironment measured with integrative optical imaging. , 1993, Biophysical journal.

[20]  F. Mora,et al.  Effects of a nitric oxide donor on glutamate and GABA release in striatum and hippocampus of the conscious rat. , 1994, Neuroreport.

[21]  O. R. Blaumanis,et al.  Evidence for a ‘Paravascular’ fluid circulation in the mammalian central nervous system, provided by the rapid distribution of tracer protein throughout the brain from the subarachnoid space , 1985, Brain Research.

[22]  J. Kerwin,et al.  The arginine‐nitric oxide pathway: A target for new drugs , 1994, Medicinal research reviews.

[23]  T. F. Freund,et al.  Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines , 1984, Neuroscience.

[24]  A. Bonci,et al.  A Common Mechanism Mediates Long-Term Changes in Synaptic Transmission after Chronic Cocaine and Morphine , 1996, Neuron.

[25]  G. Shepherd Foundations of the neuron doctrine , 1991 .

[26]  A. Privat,et al.  Localization of dopamine carriers by BTCP, a dopamine uptake inhibitor, on nigral cells cultured in vitro , 1991, Brain Research.

[27]  K. Fuxe,et al.  Aspects of neural plasticity in the central nervous system—VII. Theoretical aspects of brain communication and computation , 1990, Neurochemistry International.

[28]  D. Faber,et al.  Synergism at central synapses due to lateral diffusion of transmitter. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Gratton,et al.  Behavior-Relevant Changes in Nucleus Accumbens Dopamine Transmission Elicited by Food Reinforcement: An Electrochemical Study in Rat , 1996, The Journal of Neuroscience.

[30]  R. Mark Wightman,et al.  Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter , 1996, Nature.

[31]  K. Neve,et al.  Release of dopamine via the human transporter. , 1994, Molecular pharmacology.

[32]  E. Lábos,et al.  Non-synaptic interactions at presynaptic level , 1991, Progress in Neurobiology.

[33]  J. B. Justice,et al.  In vivo voltammetric determination of the kinetics of dopamine metabolism in the rat , 1985, Neuroscience Letters.

[34]  Anthony G. Phillips,et al.  Dopamine functions in appetitive and defensive behaviours , 1992, Progress in Neurobiology.

[35]  M. Zigmond Compensatory Neurobiological Changes after Partial Lesions with 6-Hydroxydopamine , 1994 .

[36]  J. Jefferys,et al.  Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. , 1995, Physiological reviews.

[37]  M. Häusser,et al.  Intersynaptic diffusion of neurotransmitter. , 1997, Trends in neurosciences.

[38]  C. Pennartz The ascending neuromodulatory systems in learning by reinforcement: comparing computational conjectures with experimental findings , 1995, Brain Research Reviews.

[39]  C. Nicholson,et al.  The Migration of Substances in the Neuronal Microenvironment a , 1986, Annals of the New York Academy of Sciences.

[40]  S. Mennerick,et al.  Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  T. Ichimura,et al.  Distribution of extracellular tracers in perivascular spaces of the rat brain , 1991, Brain Research.

[42]  M. Kuhar,et al.  The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  Eva Syková,et al.  The Extracellular Space in the CNS: Its Regulation, Volume and Geometry in Normal and Pathological Neuronal Function , 1997 .

[44]  G. Westbrook,et al.  The time course of glutamate in the synaptic cleft. , 1992, Science.

[45]  J. Clements Transmitter timecourse in the synaptic cleft: its role in central synaptic function , 1996, Trends in Neurosciences.

[46]  B Katz,et al.  The binding of acetylcholine to receptors and its removal from the synaptic cleft , 1973, The Journal of physiology.

[47]  L. Stjärne,et al.  Geometry, kinetics and plasticity of release and clearance of ATP and noradrenaline as sympathetic cotransmitters: Roles for the neurogenic contraction , 1995, Progress in Neurobiology.

[48]  J. Jack,et al.  Synaptic plasticity: hippocampal LTP , 1995, Current Opinion in Neurobiology.

[49]  C. Nicholson,et al.  Diffusion of albumins in rat cortical slices and relevance to volume transmission , 1996, Neuroscience.

[50]  C. Nicholson,et al.  Long distance pathways of diffusion for dextran along fibre bundles in brain. Relevance for volume transmission , 1995, Neuroreport.

[51]  T. Davis,et al.  Ectoenzymes as sites of peptide regulation. , 1996, Trends in pharmacological sciences.

[52]  Joel L. Davis,et al.  A Model of How the Basal Ganglia Generate and Use Neural Signals That Predict Reinforcement , 1994 .

[53]  K. Fuxe Dopamine receptor agonists in brain research and as therapeutic agents , 1979, Trends in Neurosciences.

[54]  E. Schuman,et al.  Synapse Specificity and Long-Term Information Storage , 1997, Neuron.

[55]  D. Armstrong,et al.  The kinetics of tubocurarine action and restricted diffusion within the synaptic cleft. , 1979, The Journal of physiology.

[56]  Marcus Jacobson,et al.  Foundations of Neuroscience , 1993, Springer US.

[57]  F. Engert,et al.  Synapse specificity of long-term potentiation breaks down at short distances , 1997, Nature.

[58]  R. Nieuwenhuys,et al.  Ultrastructural Characterization of Adrenocorticotrope Hormone (ACTH) Immunoreactive Fibres in the Mesencephalic Central Grey Substance of the Rat , 1989, The European journal of neuroscience.

[59]  J. Harvey,et al.  A Postsynaptic Interaction between Dopamine D1 and NMDA Receptors Promotes Presynaptic Inhibition in the Rat Nucleus Accumbens via Adenosine Release , 1997, The Journal of Neuroscience.

[60]  E. Kandel,et al.  Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons , 1995, Nature.

[61]  G. Edelman,et al.  The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[62]  R. Nicoll,et al.  Local and diffuse synaptic actions of GABA in the hippocampus , 1993, Neuron.

[63]  W. Schultz Dopamine neurons and their role in reward mechanisms , 1997, Current Opinion in Neurobiology.

[64]  M. Beal Oxidative Damage in Neurodegenerative Diseases , 1997 .

[65]  A. D. Smith,et al.  Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: Light and electron microscopy , 1995, Neuroscience.

[66]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  J. Schneider,et al.  Volume transmission of dopamine over large distances may contribute to recovery from experimental parkinsonism , 1994, Brain Research.

[68]  S. Young,et al.  5-hydroxydopamine-labeled dopaminergic axns: Three-dimensional reconstructions of axons, synapses and postsynaptic targets in rat neostriatum , 1994, Neuroscience.

[69]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  V. Pickel,et al.  Ultrastructural Immunocytochemical Localization of μ-Opioid Receptors in Rat Nucleus Accumbens: Extrasynaptic Plasmalemmal Distribution and Association with Leu5-Enkephalin , 1996, The Journal of Neuroscience.

[71]  R. Wightman,et al.  Control of dopamine extracellular concentration in rat striatum by impulse flow and uptake , 1990, Brain Research Reviews.

[72]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[73]  H F Cserr,et al.  Bulk flow of interstitial fluid after intracranial injection of blue dextran 2000. , 1974, Experimental neurology.

[74]  K. Fuxe,et al.  Intercellular communication in the brain: Wiring versus volume transmission , 1995, Neuroscience.

[75]  F. Gonon Prolonged and Extrasynaptic Excitatory Action of Dopamine Mediated by D1 Receptors in the Rat Striatum In Vivo , 1997, The Journal of Neuroscience.

[76]  J. Schwartz,et al.  Characterization and inhibition of a cholecystokinin-inactivating serine peptidase , 1996, Nature.

[77]  K. Chergui,et al.  Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brainin vivo , 1994, Neuroscience.