Institut für Experimentelle und Klinische Pharmakologie und Toxikologie
Albert-Ludwigs-Universität, Freiburg, Germany



Cannabinoids and synaptic transmission
The G
αi/o protein-coupled CB1 cannabinoid receptor is the primary neuronal target of the phytocannabinoid Δ9-tetrahydrocannabinol. It can also be activated by the endogenous cannabinoids (endocannabinoids) anandamide and 2-arachidonylglycerol. The CB1 receptor is widely distributed in the central nervous system. The aim of our group is to analyse the effects of exogenous and endogenous cannabinoids on synaptic transmission between identified neurons in the central nervous system. The figure below shows an example for modulation of synaptic transmission by cannabinoids. For review see Szabo and Schlicker, Handb Exper Pharmacol 168: 327-365, 2005.

Cannabinoids inhibit GABAergic synaptic transmission between basket and Purkinje cells in the cerebellar cortex. Brain slices were prepared from rat cerebellum. Spontaneously occurring action potentials (APs) in presynaptic basket cells and GABAergic inhibitory postsynaptic currents (sIPSCs) in postsynaptic Purkinje cells were recorded with the patch-clamp technique. During the initial reference period (PRE), every presynaptic AP was followed by a postsynaptic sIPSC. The synthetic CB1 cannabinoid receptor agonist WIN55212-2 inhibits synaptic transmission: now, several presynaptic action potentials are not followed by postsynaptic sIPSCs (the stars indicate these “synaptic failures”).






Hermanns-Clausen M, Kneisel S, Hutter M, Szabo B, Auwärter V (2013) Acute intoxication by synthetic cannabinoids - Four case reports. Drug Testing and Analysis DOI: 10.1002/dta.1483


Simon AC, Loverdo C, Gaffur A-L, Urbanski M, Carrel D, Rival I, Leterrier C, Benichou O, Dournaud P, Szabo B, Voituriez R, Lenkei Z (2013) Activation-dependent plasticity of polarized GPCR distribution on the neuronal surface. J Molec Cell Biol 5: 250–265


Hermanns-Clausen M, Kneisel S, Szabo B, Auwärter V (2012) Acute toxicity due to the confirmed consumption of synthetic cannabinoids: clinical and laboratory findings. Addiction 108: 534–544


Kovacs FE, Knop T, Urbanski MJ, Freiman I, Freiman TM, Feuerstein TJ, Zentner J, Szabo B (2012) Exogenous and endogenous cannabinoids suppress inhibitory neurotransmission in the human neocortex. Neuropsychopharmacology 37: 1104–1114


Kovacs FE, Illes P, Szabo B (2011) Purinergic receptor-mediated endocannabinoid production and retrograde synaptic signaling in the cerebellar cortex. Brit J Pharmacol 162: 974–988


Urbanski MJ, Kovacs FE, Szabo B (2010) Endocannabinoid-mediated synaptically evoked suppression of GABAergic transmission in the cerebellar cortex. Neuroscience 169: 1268-1278


Beetz N, Harrison MD, Brede M, Zong X, Urbanski MJ, Sietmann A, Kaufling J, Barrot M, Seeliger MW, Vieira-Coelho MA, Hamet P, Gaudet D, Seda O, Tremblay J, Kotchen TA, Kaldunski M, Nüsing R, Szabo B, Jacob HJ, Cowley Jr. AW, Biel M, Stoll M, Lohse MJ, Broeckel U, Hein L (2009) Phosducin influences sympathetic activity and prevents stress-induced hypertension in humans and mice. J Clin Invest 119: 3597-3612.


Urbanski MJ, Kovacs FE, Szabo B (2009) Depolarizing GABAergic synaptic input triggers endocannabinoid-mediated retrograde synaptic signaling. Synapse 63: 643-652.


Gilsbach R, Röser C, Beetz N, Brede M, Hadamek K, Haubold M, Leemhuis J, Philipp M, Schneider J, Urbanski M, Szabo B, Weinshenker D, Hein L (2009) Genetic dissection of α2-adrenoceptor functions in adrenergic versus non-adrenergic cells. Mol Pharmacol 75: 1160-1170.


Szabo B, Urbanski MJ, Bisogno T, Di Marzo V, Mendiguren A, Bär W and Freiman I (2006) Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol (London) 577: 263-280.


Freiman I, Anton A, Monyer H, Urbanski MJ, Szabo B (2006) Analysis of the effects of cannabinoids on identified synaptic connections in the caudate-putamen by paired recordings in transgenic mice. J Physiol (London) 575: 789-806.


Engler B, Freiman I, Urbanski M, Szabo B (2006) Effects of exogenous and endogenous cannabinoids on GABAergic neurotransmission between the caudate-putamen and the globus pallidus in the mouse. J Pharmacol Exp Ther 316: 608–617.


Freiman I, Szabo B (2005) Cannabinoids depress excitatory neurotransmission between the subthalamic nucleus and the globus pallidus. Neuroscience 133: 305-313.


Pfitzer T, Niederhoffer N, Szabo B (2005) Search for an endogenous cannabinoid-mediated effect in the sympathetic nervous system. Naunyn-Schmiedeberg´s Arch Pharmacol 371: 9-17.


Szabo B, Than M, Wallmichrath I, Thorn D (2004) Analysis of the effects of cannabinoids on synaptic transmission between basket and Purkinje cells in the cerebellar cortex of the rat. J Pharmacol Exp Ther 310: 915-925.


Pfitzer T, Niederhoffer N, Szabo B (2004) Central effects of the cannabinoid receptor agonist WIN55212-2 on respiratory and cardiovascular regulation in anaesthetised rats. Br J Pharmacol 14: 943-952.


Steffens M, Szabo B, Klar M, Rominger A, Zentner J, Feuerstein TJ (2003) Modulation of electrically evoked acetylcholine release through cannabinoid CB1 receptors: Evidence for an endocannabinoid tone in the human neocortex. Neuroscience 120: 455-465.


Schmid K, Niederhoffer N, Szabo B (2003) Analysis of the respiratory effects of cannabinoids in rats. Naunyn-Schmiedeberg´s Arch Pharmacol 368: 301-308.


Niederhoffer N, Schmid K, B Szabo (2003) The peripheral sympathetic nervous system is the major target of cannabinoids at eliciting cardiovascular depression. Naunyn-Schmiedeberg´s Arch Pharmacol 367: 434-443.


Vagts DA, Iber T, Puccini M, Szabo B, Haberstroh J, Villinger F, Geiger K, Nöldge-Schomburg GFE (2003) The effects of thoracic epidural anesthesia on hepatic perfusion and oxygenation in healthy pigs during general anesthesia and surgical stress. Anesth Analg 97: 1824-1832.


Vagts DA, Iber T, Szabo B, Haberstroh J, Reising K, Puccini M, Geiger K, Nöldge-Schomburg GFE (2003) Effects of epidural anaesthesia on intestinal oxygenation. Br J Anaesth 90: 212-220.


Szabo B, Siemes S, Wallmichrath I (2002) Inhibition of GABAergic neurotransmission in the ventral tegmental area by cannabinoids. Eur J Neurosci 15: 2057-2061.


Wallmichrath I, Szabo B (2002) Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neuroscience 113: 671-682.


Than M, Szabo B (2002) Analysis of the function of GABAB receptors on inhibitory afferent neurons of Purkinje cells in the cerebellar cortex of the rat. Eur J Neurosci 15: 1575-1584.


Wallmichrath I, Szabo B (2002) Analysis of the effect of cannabinoids on GABAergic neurotransmission in the substantia nigra pars reticulata. Naunyn-Schmiedeberg´s Arch Pharmacol 365, 326-334.


Szabo B, Fritz T, Wedzony K (2001) Effects of imidazoline antihypertensive drugs on sympathetic tone and noradrenaline release in the prefrontal cortex. Br J Pharmacol 134: 295-304


Niederhoffer N, Hansen HH, Fernandez-Ruiz JJ, Szabo B (2001) Effects of cannabinoids on adrenaline release from adrenal medullary cells. Br J Pharmacol 134: 1319-1327.


Szabo B, Nordheim U, Niederhoffer N (2001) Effects of cannabinoids on sympathetic and parasympathetic neuro-effector transmission in the rabbit heart. J Pharmacol Exp Ther 297: 819-826.


Niederhoffer N, Szabo B (2000) Cannabinoids cause central sympathoexcitation and bradycardia in rabbits. J Pharmacol Exp Ther 294: 707-713.


Szabo B, Wallmichrath I, Mathonia P, Pfreundtner C (2000) Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neuroscience 97: 89-97.


Szabo B, Müller T, Koch H (1999) Effects of cannabinoids on dopamine release in the corpus striatum and the nucleus accumbens in vitro. J Neurochem 73: 1084-1089.


Bock C, Niederhoffer N, Szabo B (1999) Analysis of the receptor involved in the central hypotensive effect of rilmenidine and moxonidine. Naunyn-Schmiedeberg´s Arch Pharmacol 359: 262-271


Niederhoffer N, Szabo B (1999) Involvement of CB1 cannabinoid receptors in the EDHF-dependent vasorelaxation in rabbits. Br J Pharmacol 126: 1383-1386


Niederhoffer N, Szabo B (1999) Effect of the cannabinoid receptor agonist WIN55212-2 on sympathetic cardiovascular regulation. Br J Pharmacol 126: 457-466


Szabo B, Bock C, Nordheim N, Niederhoffer N (1999) Mechanism of the sympathoinhibition produced by the clonidine-like drugs rilmenidine and moxonidine. Ann New York Acad Sci 881: 253-264


Szabo B, Dörner L, Pfreundtner C, Nörenberg W, Starke K (1998) Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85: 395-403.


Nörenberg W, Schöffel E, Szabo B, Starke K (1997) Subtype determination of soma-dendritic a2-autoreceptors in slices of rat locus coeruleus. Naunyn-Schmiedeberg´s Arch Pharmacol 356: 159-165


Szabo B, Urban R (1997) Role of I1 imidazoline receptors in the sympathoinhibition produced by intracisternally administered rilmenidine and moxonidine. Drug Res 47 (II): 1009-1015


Szabo B, Fröhlich R, Illes P (1996) No evidence for functional imidazoline receptors on locus coeruleus neurons. Naunyn-Schmiedeberg´s Arch Pharmacol 353: 557-563


Driessen B, Concalves J, Szabo B (1996) Failure of tyramine to release neuronal ATP as a cotransmitter of noradrenaline in the guinea-pig vas deferens. Naunyn-Schmiedeberg´s Arch Pharmacol 353: 175-183


Szabo B, Urban R (1995) Mechanism of sympathoinhibition by imidazolines. Ann New York Acad Sci 763: 552-565


Urban R, Szabo B, Starke K (1995) Involvement of peripheral presynaptic inhibition in the reduction of sympathetic tone by moxonidine, rilmenidine and UK 14304. Eur J Pharmacol 282: 29-37


Urban R, Szabo B, Starke K (1995) Involvement of a2-adrenoceptors in the cardiovascular effects of moxonidine. Eur J Pharmacol 282: 19-28


Cassel JC, Jeltsch H, Neufang B, Lauth D, Szabo B, Jackisch R (1995) Downregulation of muscarinic- and 5-HT1B-receptor-mediated modulation of [3H]-acetylcholine release in brain slices of rats with fimbria-fornix lesions and intrahippocampal grafts of septal origin. Brain Res 704: 153-166


Szabo B, Urban R, Starke K (1995) Cardiovascular effects of agmatine, a "clonidine-displacing substance", in conscious rabbits. Naunyn-Schmiedeberg´s Arch Pharmacol 351: 268-273


Szabo B, Obergfell A, Starke K (1995) Involvement of monoamine uptake inhibition and local anesthesia in the cardiovascular response to cocaine in conscious rabbits. J Pharmacol Exp Ther 273: 128-137


Urban R, Szabo B, Starke K (1994) Is the sympathoinhibitory effect of rilmenidine mediated by alpha-2 adrenoceptors or imidazoline receptors? J Pharmacol Exp Ther 270: 572-578


Szabo B, Urban R, Starke K (1993) Sympathoinhibition by rilmenidine in conscious rabbits: involvement of a2-adrenoceptors. Naunyn-Schmiedeberg´s Arch Pharmacol 348: 593-600


Szabo B, Auberle T, Starke K (1993) Inhibition of uptake1 by (+)-oxaprotiline reveals a differential central regulation of noradrenaline and adrenaline release. Naunyn-Schmiedeberg´s Arch Pharmacol 348: 249-257


Bültman R, Szabo B, Starke K (1993) Inhibition by ethanol of contractions of rat vas deferens: no evidence for selective blockade of P2x-purinoceptors. Naunyn-Schmiedeberg´s Arch Pharmacol 347: 527-533


Szabo B, Schramm A, Starke K (1992) Effect of yohimbine on renal sympathetic nerve activity and renal norepinephrine spillover in anesthetized rabbits. J Pharmacol Exp Ther 260: 780-788


Szabo B, Karsch V, Starke K (1992) Effects of inhibitors of neuronal uptake of 5-HT on sympathetic cardiovascular regulation. J Cardiovasc Pharmacol 20: 99-107


Szabo B, Crass D, Starke K (1992) Effect of the dopamine D2 receptor agonist quinpirole on renal sympathetic nerve activity and renal norepinephrine spillover in anesthetized rabbits. J Pharmacol Exp Ther 263: 806-815


Szabo B, Schultheiss A, Starke K (1991) The noradrenaline uptake inhibitor, (+)-oxaprotiline, but not the inactive enantiomer, (-)-oxaprotiline, inhibits sympathetic nerve activity in the rabbit: involvement of adrenoceptors. Eur J Pharmacol 199: 325-334


Meyer DK, Holland A, Lais A, Szabo B (1991) Effects of p-chloroamphetamine on release of [3H]gamma-aminobutyric acid from slices of rat caudate-putamen. Eur J Pharmacol 196: 189-195


Szabo B, Schultheiss A (1990) Desipramine inhibits sympathetic nerve activity in the rabbit. Naunyn-Schmiedeberg's Arch Pharmacol 342: 469-476


Szabo B, Hedler L, Schurr C, Starke K (1990) Peripheral presynaptic facilitatory effect of angiotensin II on noradrenaline release in anesthetized rabbits. J Cardiovasc Pharmacol 15: 968-975


Szabo B, Hedler L, Starke K (1989) Facilitation of the release of noradrenaline: an extraadrenal effect of adrenocorticotropic hormone. Resuscitation 18: 229-242


Szabo B, Hedler L, Starke K (1989) Peripheral presynaptic and central effects of clonidine, yohimbine and rauwolscine on the sympathetic nervous system in rabbits. Naunyn-Schmiedeberg's Arch Pharmacol 340: 648-657


Szabo B, Hedler L, Schurr C, Starke K (1988) Peripheral sympatho-inhibitory cardiovascular effects of opioid peptides in anaesthetized rabbits. Br J Pharmacol 94: 781-788


Szabo B, Hedler L, Schurr C, Starke K (1988) ACTH increases nordrenaline release in the rabbit heart. Naunyn-Schmiedeberg's Arch Pharmacol 338: 368-372


Szabo B, Wichmann T, Starke K (1987) Presynaptic opioid receptors in the portal vein of the rabbit. Eur J Pharmacol 139: 103-110


Szabo B, Hedler L, Lichtwald K, Starke K (1987) ACTH increases noradrenaline release in pithed rabbits with electrically stimulated sympathetic outflow. Eur J Pharmacol 136: 391-399


Acs Zs, Szabo B, Kapocs G, Makara GB (1987) g-Aminobutyric acid stimulates pituitary growth hormone secretion in the neonatal rat. A superfusion study. Endocrinology 120: 1790-1798


Szabo B, Hedler L, Starke K (1986) Dopamine receptor agonist and alpha-2 adrenoceptor antagonist effects of fenoldopam in rabbits. J Pharmacol Exp Ther 239: 881-886


Szabo B, Hedler L, Ensinger H, Starke K (1986) Opioid peptides decrease noradrenaline release and blood pressure in the rabbit at peripheral receptors. Naunyn-Schmiedeberg's Arch Pharmacol 332: 50-56


Ensinger H, Hedler L, Szabo B, Starke K (1986) Bremazocine causes sympatho-inhibition and hypotension in rabbits by activating peripheral k-receptors. J Cardiovasc Pharmacol 8: 470-475


Enyedi P, Szabo B, Spät A (1985) Reduced responsiveness of glomerulosa cells after prolonged stimulation with angiotensin II. Am J Physiol 248: E209-E214


Enyedi P, Szabo B, Spät A (1983) Failure of vasoactive intestinal polypeptide to stimulate aldosterone production. Acta Physiol Hung 61: 77-79




Szabo B, Schlicker E (2005) Effects of cannabinoids on neurotransmission. In: Pertwee RG (Ed.) Cannabinoids, Handbook of Experimental Pharmacology, Vol. 168, pp 327-365, Springer, Berlin.


Wallmichrath I, Szabo B (2004) Cannabinoide und neuronale Signalübertragung. Sucht 50: 297-308.


Szabo B (2002) Imidazoline antihypertensive drugs - a critical review on their mechanism of action. Pharmacol Ther 93: 1-35.


Szabo B, Niederhoffer N (1998) Effects of cannabinoids on cardiovascular regulation in rabbits. Pharmacol Toxicol 83 (suppl. I): 87-89




Wallmichrath I, Szabo B (2004) Influence of exogenous and endogenous cannabinoids on synaptic transmission. In: Wenger T (Ed.) Recent advances in pharmacology and physiology of cannabinoids, pp.75-96. Research Signpost, Kerala


Szabo B, Wallmichrath I (2003) Cannabinoide und die Kommunikation zwischen Neuronen. In: Fischer J (Ed.) Weggefährten, pp. 218-249. Pabst Science Publishers, Berlin


Szabo B, Wallmichrath I, Niederhoffer N (2002) Wirkungen von Cannabinoiden auf Neurone. In: Richter G, Rommelspacher H, Spies C (Eds.) "Alkohol, Nikotin, Kokain... und kein Ende?", pp. 387-394. Pabst Science Publishers, Berlin


Szabo B (2002) A szimpatikus idegrendszer gyógyszeres befolyásolása (auf Deutsch: Pharmakologische Beeinflussung des sympathischen Nervensystems). In: Vizi E-Sz (Ed.) Humán farmakológia: a racionális gyógyszerterápia alapjai (auf Deutsch: Humanpharmakologie: Grundlagen der rationalen Pharmakotherapie), pp. 440-452. Medicina, Budapest


Schultheiss A, Szabo B, Starke K (1991) Inhibition of NA uptake by (+)-oxaprotiline inhibits sympathetic nerve activity. In: Langer SZ, Galzin AM, Costentin J (Eds.) Advances in the biosciences, Presynaptic receptors and neuronal transporters, Vol. 82, pp. 327-328. Pergamon, Oxford


Szabo B, Ramme D, Starke K (1988) Opioid receptors in the sympathetic supply to blood vessels and the heart. In: Stumpe KO, Kraft K, Faden AI (Eds.) Opioid peptides and blood pressure control, pp. 129-140. Springer, Berlin


Starke K, Illes P, Ramme D, Ensinger H, Hedler L, Szabo B, von Kügelgen I, Pfeiffer N, Limberger N (1987) Peripheral pre-junctional opioid receptors in cardiovascular control. In: Nobin A, Owman C, Arneklo-Nobin B (Eds.) Neuronal messengers in vascular function, pp. 247-269. Elsevier, Amsterdam


Starke K, Majewski H, Ensinger H, Szabo B, Hedler L (1986) In vivo operation of prejunctional adrenoceptors in the peripheral sympathetic nervous system. In: Grobecker H, Philippu A, Starke K (Eds.) New aspects of the role of adrenoceptors in the cardiovascular system, pp. 43-56. Springer, Berlin


Members of the group

Bela Szabo
Ilka Freiman
Flora Kovacs, Mario Lederer, Sophia Linder, Holger Schwarz, Tim Knop, Marco Spehl
Previous: Michal Urbanski, Wolfram Bär

Professor Dr. med. Bela Szabo

Telefon: +49-761-203-5312
Fax: +49-761-203-5318
Curriculum vitae
List of publications

Dr. Bela Szabo - Curriculum vitae


Szabo, Bela; MD, professor


1957 in Budapest, Hungary


D-79104 Freiburg i. Br., Germany


Until 1994 Hungarian; since 1995 German

Schools and University


Elementary school in Budapest


Secondary school at the church order "Scolae Piae" in Budapest


Ambulance officer at the Hungarian Ambulance Service


Study of medicine at the Semmelweis Medical University in Budapest


Participation in the research and teaching activity of the Physiological Department of the Semmelweis University


Completion of the medical studies with the mark "summa cum laude". Physician´s licence for Hungary ("Approbation")

Scientific development


Junior scientist in the Medical Research Institute of the Hungarian Academy of Sciences


Guest scientist in the Department of Pharmacology of the Albert-Ludwig University in Freiburg


Junior scientist in the Department of Pharmacology of the Albert-Ludwig University in Freiburg


MD thesis completion in the Department of Pharmacology of the Albert-Ludwig University in Freiburg; mark: "magna cum laude"


Postdoctoral fellow in the Department of Pharmacology of the Albert-Ludwig University in Freiburg; training as a specialist in Pharmacology and Toxicology

Since 1995

Physician´s licence for Germany ("Approbation")


Specialist´s certification for Pharmacology and Toxicology ("Facharzt")


PhD ("Habilitation") for Pharmacology and Toxicology


Reader ("Hochschuldozent; C2") in the Department of Pharmacology of the Albert-Ludwig University in Freiburg


Professor ("außerplanmäßiger Professor")

Memberships in scientific organizations

Since 1983

Member of the Hungarian Physiological Society

Since 1990

Member of the German Society for Experimental and Clinical Pharmacology and Toxicology

Since 1996

Member of the Working Group for Neuropharmacology and -Toxicology (within the German Society for Experimental and Clinical Pharmacology and Toxicology)

Since 1998

Member of the International Cannabinoid Research Society

Since 1999

Advisory editor at Naunyn-Schmiedeberg´s Archives of Pharmacology

Since 2009

Member of the Review Editorial Board at Frontiers in Systems Neuroscience


Dr. rer. nat. Ilka Freiman, postdoctoral fellow

Flora Kovacs, PhD student (recipient of a DAAD scholarship)






Mario Lederer, PhD student



Sophia Linder, medical PhD student

Tim Knop, medical PhD student




Holger Schwarz, medical PhD student



Marco Spehl, medical PhD student

Previous member: Dr. rer. nat. Michal Urbanski

Present address:
Department of Biological Sciences
Room HN834 Hunter College of City University
New York, NY 10065, USA
Phone: 00-1-212- 772-5295



Previous member: Dr. rer. nat. Wolfram Bär



Institut für Experimentelle und Klinische Pharmakologie und Toxikologie
Albertstrasse 25
D-79104 Freiburg i. Br.
Telefon: +49-761-203-5312
Fax: +49-761-203-5318


Photo gallery

Patch-clamp setup

Bicycle excursion to Kandel in the Black Forest (2003)

Preparing for a bike excursion to Föhrental in the Black Forest (2003)

Before a bike tour to Waldkirch in the Black Forest (2004)

At the Second European Workshop on Cannabinoids (Busto Arsizio in Italy, 2005)

Climbing to the peak of Belchen in the Black Forest (2007)

Rothenbachkopf in the Vosges (2010)

Schlittschuhlaufen auf dem Eglisee in Basel (2014)


Meaning of life