Research Topics
Genomes and Genes | R H EdwardsSummaryAffiliation: University of California Country: USA Publications
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Publications
Drug delivery via the blood-brain barrierR H Edwards
Graduate Programs in Neuroscience, Cell Biology and Biomedical Sciences and the Departments of Neurology and Physiology, UCSF School of Medicine, 513 Parnassus Avenue, San Francisco, California 94143 0435, USA
Nat Neurosci 4:221-2. 2001..The blood-brain barrier forms a buffer against the systemic circulation. Now drugs administered to the brain are shown to be exported by a transporter to act at peripheral sites...- Neurotransmitter release: variations on a themeR H Edwards
Departments of Neurology and Physiology, UCSF School of Medicine, 513 Parnassus Avenue, San Francisco, California 94143 0435, USA
Curr Biol 8:R883-5. 1998..Similarities between the ways that synaptic vesicles and large dense-core vesicles release their contents have been emphasized, but recent studies have revealed important mechanistic differences between these two exocytotic processes... - The expression of vesicular glutamate transporters defines two classes of excitatory synapseR T Fremeau
Department of Neurology, Graduate Program in Neuroscience, UCSF School of Medicine, San Francisco, CA 94143, USA
Neuron 31:247-60. 2001..Like VGLUT1, this protein localizes to synaptic vesicles and functions as a vesicular glutamate transporter (VGLUT2). The complementary expression of VGLUT1 and 2 defines two distinct classes of excitatory synapse... 
Coupled and uncoupled proton movement by amino acid transport system NF A Chaudhry
Department of Neurology, Graduate Program in Neuroscience, UCSF School of Medicine, 513 Parnassus Avenue, San Francisco, CA 94143-0435, USA
EMBO J 20:7041-51. 2001..Protons thus permeate SN1 both coupled to and uncoupled from amino acid flux, providing novel mechanisms to regulate the transfer of glutamine between cells...- An acidic motif retains vesicular monoamine transporter 2 on large dense core vesiclesC L Waites
Graduate Program in Neuroscience, Department of Neurology, University of California, San Francisco School of Medicine, San Francisco, California 94143-0435, USA
J Cell Biol 152:1159-68. 2001..Phosphorylation of the acidic cluster thus appears to reduce the localization of VMAT2 to LDCVs by inactivating a retention mechanism... - The essence of excitationR J Reimer
Departments of Neurology and Physiology, Graduate Programs in Neuroscience, Cell Biology and Biomedical Sciences, University of California, San Francisco, School of Medicine, 513 Parnassus Avenue, 94143-0435, USA
Curr Opin Cell Biol 13:417-21. 2001..Recent advances in our understanding of glutamate storage and release now illuminate how this ubiquitous amino acid can function as a signalling molecule... - Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporterE E Bellocchio
Department of Neurology, University of California at San Francisco School of Medicine, 513 Parnassus Avenue, San Francisco, CA 94143 0435, USA
Science 289:957-60. 2000..In addition, we show that this vesicular glutamate transporter, VGLUT1, exhibits a conductance for chloride that is blocked by glutamate... - Amino acid transport system A resembles system N in sequence but differs in mechanismR J Reimer
Department of Neurology, University of California, San Francisco School of Medicine, 513 Parnassus Avenue, San Francisco, CA 94143
Proc Natl Acad Sci U S A 97:7715-20. 2000..Transport mediated by SA1 is also electrogenic. Amino acid transport Systems A and N thus appear closely related in function as well as structure, but exhibit important differences in ionic coupling... - Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmissionF A Chaudhry
Department of Neurology, UCSF School of Medicine, San Francisco, California 94143 0435, USA
Cell 99:769-80. 1999..Together with the pattern of SN1 expression, these unusual properties suggest novel physiological roles for system N in nitrogen metabolism and synaptic transmission... - Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivoThomas S Hnasko
Departments of Physiology and Neurology, University of California, San Francisco, San Francisco, CA 94158, USA
Neuron 65:643-56. 2010..Remarkably, low concentrations of glutamate acidify synaptic vesicles more slowly but to a greater extent than equimolar Cl(-), indicating a distinct, presynaptic mechanism to regulate quantal size... - VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamateRobert T Fremeau
Department of Neurology, Graduate Program in Neuroscience, UCSF School of Medicine, 600 16th Street, San Francisco, CA 94143 2140, USA
Trends Neurosci 27:98-103. 2004..VGLUT3 also differs from VGLUT1 and VGLUT2 in its subcellular location, with somatodendritic as well as axonal expression... - Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3Rebecca P Seal
Department of Physiology, School of Medicine, University of California, San Francisco, San Francisco, CA 94143, USA
Neuron 57:263-75. 2008..The glutamate release conferred by expression of VGLUT3 thus has an essential role in both function and development of the auditory pathway, as well as in the control of cortical excitability... - Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamateGarret D Stuber
Ernest Gallo Clinic and Research Center, University of California, San Francisco, Emeryville, California 94608, USA
J Neurosci 30:8229-33. 2010..Thus, the unique ability of NAc-projecting dopamine neurons to synchronously activate both dopamine and glutamate receptors may have crucial implications for the ability to respond to motivationally significant stimuli... - Glutamine uptake by neurons: interaction of protons with system a transportersFarrukh A Chaudhry
Department of Neurology, University of California San Francisco School of Medicine, San Francisco, California 94143-0435, USA
J Neurosci 22:62-72. 2002..Differences between System N and A transporters in coupling to H+ thus contribute to the delivery of glutamine from glia to neurons. Nonetheless, although they are not transported, H+ inhibit SA1 and SA2 by competing with Na+... - Identification and characterization of the vesicular GABA transporterS L McIntire
Graduate Programs in Neuroscience, Cell Biology and Biomedical Sciences, Department of Neurology, UCSF School of Medicine, San Francisco, California 94143 0435, USA
Nature 389:870-6. 1997..Thus VGAT is the first of a new family of neurotransmitter transporters... - Functional implications of neurotransmitter co-release: glutamate and GABA share the loadRebecca P Seal
Department of Neurology, UCSF School of Medicine, 600 16th St, GH-N272B, San Francisco, CA 94143-2140, USA
Curr Opin Pharmacol 6:114-9. 2006..Moreover, dynamic regulation of neurotransmitter phenotypes increases the plasticity of neurotransmission, indicating potential avenues for therapeutic intervention... - Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retinaJuliette Johnson
Department of Ophthalmology, University of California School of Medicine, San Francisco, San Francisco, California 94143, USA
J Comp Neurol 477:386-98. 2004..Furthermore, a subset of VGLUT3 cells expressed the circadian clock gene period 1, implicating VGLUT3 cells as part of the light-entrainable retina-based circadian system... - Vesicular glutamate transporter 1 is required for photoreceptor synaptic signaling but not for intrinsic visual functionsJuliette Johnson
Department of Ophthalmology, University of California School of Medicine, San Francisco, California 94143, USA
J Neurosci 27:7245-55. 2007..Furthermore, melanopsin and VGLUT2 expression in a subset of RGCs immediately after birth strongly supports the idea that intrinsic vision can function well before rod- and cone-mediated signaling has matured... - The neurotransmitter cycle and quantal sizeRobert H Edwards
Department of Neurology and Physiology, UCSF School of Medicine, San Francisco, CA 94158 2517, USA
Neuron 55:835-58. 2007..This review will summarize current understanding of the neurotransmitter cycle and indicate basic, unanswered questions about the presynaptic regulation of quantal size... - Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosisVenu M Nemani
Departments of Neurology and Physiology, Graduate Program in Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA
Neuron 65:66-79. 2010..Increased levels of alpha-synuclein thus produce a specific, physiological defect in synaptic vesicle recycling that precedes detectable neuropathology... - Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamateJuliette Johnson
Department of Ophthalmology, University of California School of Medicine, San Francisco, California 94143 0730, USA
J Neurosci 23:518-29. 2003..Furthermore, vesicular glutamate transmission likely occurs before ribbon synapse formation in the inner retina... - Vesicular transport regulates monoamine storage and release but is not essential for amphetamine actionE A Fon
Department of Neurology, UCSF School of Medicine, University of California, San Francisco 94143, USA
Neuron 19:1271-83. 1997.... - Synaptic vesicles: half full or half empty?Thomas S Hnasko
Department of Neurology, School of Medicine, University of California San Francisco, 600 16th Street, GH N272B, San Francisco, CA 94158, USA
Neuron 51:523-4. 2006..In this issue of Neuron, Prado et al. pursue this line of investigation and show that changes in transporter expression that alter quantal size can affect behavior... - Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recyclingSusan M Voglmaier
Department of Neurology, Graduate Programs in Cell Biology, Neuroscience and Biomedical Sciences, UCSF School of Medicine, 600 16th Street, San Francisco, California 94143, USA
Neuron 51:71-84. 2006..After stimulation, however, inhibition of the AP3 pathway prevents the full recovery of VGLUT1 by endocytosis, implicating the AP3 pathway specifically in compensatory endocytosis... - Neural activity controls the synaptic accumulation of alpha-synucleinDoris L Fortin
Department of Neurology, Graduate Program in Biomedical Sciences, University of California, San Francisco, California 94143-2140, USA
J Neurosci 25:10913-21. 2005..Furthermore, the dispersion of alpha-synuclein is graded with respect to stimulus intensity. Neural activity thus controls the normal function of alpha-synuclein at the nerve terminal and may influence its role in PD... - The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamateRobert T Fremeau
Department of Neurology, University of California School of Medicine, San Francisco, CA 94143, USA
Proc Natl Acad Sci U S A 99:14488-93. 2002..The dendritic expression of VGLUT3 by particular neurons also indicates the potential for retrograde synaptic signaling. The distribution and subcellular location of VGLUT3 thus suggest novel modes of signaling by glutamate... - The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmissionE E Bellocchio
Departments of Neurology and Physiology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, San Francisco, California 94143, USA
J Neurosci 18:8648-59. 1998..Expression of BNPI on synaptic vesicles suggests a mechanism for neural activity to regulate the function of BNPI... - Do different endocytic pathways make different synaptic vesicles?Susan M Voglmaier
Department of Psychiatry, UCSF School of Medicine, 600 16th Street, San Francisco, CA 94158 2517, USA
Curr Opin Neurobiol 17:374-80. 2007..These observations might begin to account for differences in the properties of different vesicle pools... - Vesicular monoamine and glutamate transporters select distinct synaptic vesicle recycling pathwaysBibiana Onoa
Department of Neurology, University of California, San Francisco School of Medicine, San Francisco, California 94158 2517, USA
J Neurosci 30:7917-27. 2010..Even when expressed in the same neuron, the two vesicular transporters thus target to distinct populations of synaptic vesicles, presumably due to their selection of distinct recycling pathways... - The H+-coupled electrogenic lysosomal amino acid transporter LYAAT1 localizes to the axon and plasma membrane of hippocampal neuronsChristopher C Wreden
Department of Neurology and Physiology, University of California San Francisco School of Medicine, San Francisco, California 94143 0435, USA
J Neurosci 23:1265-75. 2003..A protease protection assay and measurements of intracellular pH further indicate abundant expression at the plasma membrane, raising the possibility of physiological roles for LYAAT1 on the cell surface as well as in lysosomes... - The effect of rare human sequence variants on the function of vesicular monoamine transporter 2Jonathon Burman
Department of Neurology, UCSF School of Medicine, San Francisco, CA 94143 2140, USA
Pharmacogenetics 14:587-94. 2004..The results illustrate the relationship between conservation of the affected residue, the nature of the substitution and effects on substrate versus inhibitor interaction... 
Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondriaKen Nakamura
Graduate Program in Neuroscience, Department of Neurology, University of California at San Francisco, San Francisco, California 94143, USA
J Neurosci 28:12305-17. 2008..We find that the conformation of alpha-synuclein responds selectively to mitochondria, indicating a direct link between alpha-synuclein and an organelle strongly implicated in the pathogenesis of PD...- The glutamine commute: take the N line and transfer to the AFarrukh A Chaudhry
Graduate Program in Neuroscience, Department of Neurology, University of California at San Francisco School of Medicine, San Francisco, CA 94143, USA
J Cell Biol 157:349-55. 2002.... - Lipid rafts mediate the synaptic localization of alpha-synucleinDoris L Fortin
Department of Neurology, Graduate Programs in Biomedical Sciences, Cell Biology and Neuroscience, University of California San Francisco School of Medicine, San Francisco, California 94143 2140, USA
J Neurosci 24:6715-23. 2004.... - Sorting of vesicular monoamine transporter 2 to the regulated secretory pathway confers the somatodendritic exocytosis of monoaminesHaiyan Li
Graduate Programs in Neuroscience and Cell Biology, Department of Neurology and Physiology, UCSF School of Medicine, 600 16th Street, San Francisco, California 94143, USA
Neuron 48:619-33. 2005..VMAT2 thus defines a population of secretory vesicles that mediate the activity-dependent somatodendritic release of multiple retrograde signals involved in synaptic function, growth, and plasticity... - Thyronamines inhibit plasma membrane and vesicular monoamine transportAaron N Snead
Graduate Program in Chemistry and Chemical Biology, University of California at San Francisco, San Francisco, California 94143, USA
ACS Chem Biol 2:390-8. 2007..These observations expand the nontranscriptional role of thyroid hormone derivatives and may help to explain the pharmacological effects of thyronamines in vivo... - Physiology versus pathology in Parkinson's diseaseKen Nakamura
Departments of Neurology and Physiology, University of California School of Medicine, 600 16th Street, GH-N272B, San Francisco, CA 94158-2517, USA
Proc Natl Acad Sci U S A 104:11867-8. 2007 - A combinatorial code for the interaction of alpha-synuclein with membranesShin Ichiro Kubo
Department of Neurology, Graduate Program in Biomedical Sciences, University of California, San Francisco, California 94143 2140, USA
J Biol Chem 280:31664-72. 2005.... - Secretion of L-glutamate from osteoclasts through transcytosisRiyo Morimoto
Laboratory of Membrane Biochemistry, Okayama University Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama, Japan
EMBO J 25:4175-86. 2006..Glutamate signaling may play an important role in the bone homeostasis... - Complementary distribution of type 1 cannabinoid receptors and vesicular glutamate transporter 3 in basal forebrain suggests input-specific retrograde signalling by cholinergic neuronsTibor Harkany
Laboratory of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Scheeles väg 1 A1, Karolinska Institutet, S 17177 Stockholm, Sweden
Eur J Neurosci 18:1979-92. 2003.... - Expression of plasma membrane GABA transporters but not of the vesicular GABA transporter in dentate granule cells after kainic acid seizuresGunther Sperk
Department of Pharmacology, University of Innsbruck, Innsbruck, Austria
Hippocampus 13:806-15. 2003..GABA could then act on GABA-A receptors, protecting granule cells from overexcitation... - Complementary distribution of vesicular glutamate transporters 1 and 2 in the nucleus accumbens of rat: Relationship to calretinin-containing extrinsic innervation and calbindin-immunoreactive neuronsWolfgang Hartig
Paul Flechsig Institute for Brain Research, University of Leipzig, D 04109 Leipzig, Germany
J Comp Neurol 465:1-10. 2003.... - Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root gangliaAlexandre L R Oliveira
Department of Neuroscience, The Retzius Laboratory, Karolinska Institutet, SE-171 77 Stockholm, Sweden
Synapse 50:117-29. 2003..VGLUT1 is mainly present in primary afferents from large, CGRP-negative DRG neurons, VGLUT2 has mainly a local origin, and VGLUT3 fibers probably have a supraspinal origin... - Vesicular neurotransmitter transporters as targets for endogenous and exogenous toxic substancesFarrukh A Chaudhry
Centre for Molecular Biology and Neuroscience, The Biotechnology Centre of Oslo, University of Oslo, Oslo, Norway
Annu Rev Pharmacol Toxicol 48:277-301. 2008..Thus, specific inhibitors have helped to characterize both the physiological role and mechanism of vesicular neurotransmitter transport... - Postnatal development of the glutamate vesicular transporter VGLUT1 in rat cerebral cortexAndrea Minelli
Istituto di Fisiologia Umana, Universita di Ancona, Via Tronto 10 A, Torrette di Ancona, I 60020, Ancona, Italy
Brain Res Dev Brain Res 140:309-14. 2003..Its spatial and temporal maturation patterns suggest that VGLUT1 may be the vesicular transporter in developing corticocortical connections... - Methamphetamine-induced degeneration of dopaminergic neurons involves autophagy and upregulation of dopamine synthesisKristin E Larsen
Department of Neurology, Columbia University, and New York Psychiatric Institute, New York, New York 10032, USA
J Neurosci 22:8951-60. 2002.... - Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycleJean-Luc Boulland
Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, P.O. Box 1105 Blindern, Norway
Eur J Neurosci 15:1615-31. 2002.... - Regulation of the glutamine transporter SN1 by extracellular pH and intracellular sodium ionsAngelika Bröer
School of Biochemistry and Molecular Biology, Australian National University, Canberra ACT 0200, Australia
J Physiol 539:3-14. 2002..A slippage mode in the transporter mechanism and pH-regulated endogenous oocyte cation channels are likely to contribute to the observed currents... - Electrochemical monitoring of transport by a vesicular monoamine transporter expressed in Xenopus oocytesJanet Whitley
Medical Science, Indiana University School of Medicine, Jordan Hall 104, Bloomington, IN 47405-6401, USA
J Neurosci Methods 133:191-9. 2004..These results suggest that expression of VMATs in oocytes may provide a useful model system for mechanistic and regulatory studies that would not be feasible using traditional methods... - Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosisKristin E Larsen
Department of Neurology, Columbia University School of Medicine, New York, New York 10032, USA
J Neurosci 26:11915-22. 2006..We conclude that alpha-syn overexpression inhibits a vesicle "priming" step, after secretory vesicle trafficking to "docking" sites but before calcium-dependent vesicle membrane fusion... - Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sitesRobert T Fremeau
Department of Neurology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, CA 94143, USA
Science 304:1815-9. 2004..The loss of VGLUT1 also reduced the reserve pool of synaptic vesicles. Thus, VGLUT1 plays an unanticipated role in membrane trafficking at the nerve terminal... - Endocannabinoid-independent retrograde signaling at inhibitory synapses in layer 2/3 of neocortex: involvement of vesicular glutamate transporter 3Tibor Harkany
Unit of Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Karolinska Institutet, S-17177 Stockholm, Sweden
J Neurosci 24:4978-88. 2004.... - Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weightMaria Collin
Department of Neuroscience, Karolinska Institutet, , B3, 5th Floor, Room 514, SE-171 77 Stockholm, Sweden
Eur J Neurosci 18:1265-78. 2003.... - Vesicular glutamate transporter 3 (VGLUT3) identifies spatially segregated excitatory terminals in the rat substantia nigraRaquel Martín-Ibáñez
Laboratory for Molecular Neurobiology, Department of Medical Biochemistry and Biophysics, Scheeles väg 1 A1
Eur J Neurosci 23:1063-70. 2006..Collectively, our data indicate that VGLUT3 identifies a novel excitatory terminal subset that contributes to the tuning of DA cell excitability in the substantia nigra... - Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmittersJean-Luc Boulland
Institute of Basic Medical Sciences and the Centre for Molecular Biology and Neuroscience, University of Oslo, N-0317 Oslo, Norway
J Comp Neurol 480:264-80. 2004..In skeletal muscle, VGLUT3 localizes to granular organelles in the axon terminal as well as in the muscle sarcoplasm. The results suggest novel mechanisms and roles for regulated transmitter release... - Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout miceBenjamin G Croft
Centre for Neuronal Survival and Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec H3A 2B4, Canada
Mol Biol Cell 16:306-15. 2005.... - Evidence that certain retinal bipolar cells use both glutamate and GABAYen Hong Kao
Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104 6058, USA
J Comp Neurol 478:207-18. 2004..By "targeted injection," we identified two types of OFF bipolar cell with the machinery to make and package both transmitters. One of these types costratifies with a dopamine plexus... - Fast subplasma membrane Ca2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytesJulie Marchaland
Department of Cell Biology and Morphology, Faculty of Biology and Medicine, University of Lausanne, 1005 Lausanne, Switzerland
J Neurosci 28:9122-32. 2008..Overall, the above characteristics of transmitter exocytosis from astrocytes support a role of this process in fast synaptic modulation... - Organic anion transport is the primary function of the SLC17/type I phosphate transporter familyRichard J Reimer
Department of Neurology and Neurological Sciences, Stanford University School of Medicine, CA 94305, Stanford, USA
Pflugers Arch 447:629-35. 2004.... - Changes in purinergic signaling after cerebral injury -- involvement of glutamatergic mechanisms?Heike Franke
Rudolf Boehm Institute of Pharmacology and Toxicology, University of Leipzig, Leipzig, Germany
Int J Dev Neurosci 24:123-32. 2006..It can be assumed, that the enhanced sensitivity of neurons to purinergic signaling may be related directly or indirectly to changes of the glutamatergic transmission... - Distribution of vesicular glutamate transporters 1 and 2 in the rat spinal cord, with a note on the spinocervical tractStefan Persson
Department of Experimental Medical Science, Division for Neuroscience, and Lund University Pain Research Center, Lund University, S 221 84 Lund, Sweden
J Comp Neurol 497:683-701. 2006..The mediolateral differences in VGLUT1 distribution in laminae I-II suggest dual origins of VGLUT1-immunoreactive varicosities in this region... - Antidepressants and the monoamine masqueradeDavid Sulzer
Department of Neurology, Columbia University, New York State Psychiatric Institute, New York, New York 10032, USA
Neuron 46:1-2. 2005..The results suggest that release of serotonin by dopamine neurons may contribute to the effects of multiple major classes of antidepressants...
Research Grants
- New Perspectives in Transporter Biology-FASEB conferenceRobert Edwards; Fiscal Year: 2003..Each oral session will be followed by a panel discussion of the topic. To promote the advancement of junior faculty, the most exciting poster submissions will be selected for short oral presentations during the regular oral sessions. ..
- TRANSPORT OF NEUROTRANSMITTERS INTO SYNAPTIC VESICLESRobert Edwards; Fiscal Year: 2005..Third, we will manipulate the expression, localization and regulation of the transporters in vivo to assess the role of these mechanisms in synaptic transmission and behavior. ..
- TRANSPORT OF NEUROTRANSMITTER INTO SYNAPTIC VESICLESRobert Edwards; Fiscal Year: 2007..We will also produce a conditional knock-out to distinguish among the behavioral effects of VGLUTS expressed by different neurons. ..