The Bekkers Group - Olfaction

We are interested in how the mammalian brain processes sensory information received from the external world. Although the nature of this information varies between the different senses (vision, touch, smell, etc.), there are remarkable similarities in how the different sensory features are encoded in the cerebral cortex. Thus, it is likely that it will be possible to uncover general principles about brain operation that underlie all cortical sensory processing.  For this reason, we have chosen to focus on the olfactory system because olfaction is a primitive sense with a relatively simple anatomy. Moreover, compared to the other senses, olfaction is virgin territory. Smell remains our most enigmatic sense.

Our research focuses in particular on the primary olfactory cortex, also called the piriform cortex, which is located in the basal forebrain just behind the nose. The piriform cortex is the first cortical destination of olfactory information and is thought to be important for recognising and remembering odours as holistic 'odour images', i.e. as 'rose' or 'chocolate' rather than as a simple list of chemical components. How the piriform cortex achieves this astonishing feat, despite its comparatively simple structure, is a major aim of our research.  The piriform cortex is also highly epileptic and is involved in amplifying seizures in humans.  Some of our research examines why the piriform cortex is so susceptible to epilepsy, with implications for the development of new anti-epileptic drugs.

Our experiments use a variety of cutting-edge techniques, including patch clamp electrophysiology in vivo and in vitro, 2-photon microscopy, optogenetics and neural network modelling. For example, one project uses 2-photon calcium imaging in anaesthetised mice to map neuronal activity in the piriform cortex in response to odour applications to the nose.  Another project uses patch clamping and imaging in slices to explore the properties of circuits in the piriform cortex that may give rise to epilepsy.  In the longer term, our work will reveal the essential components of this prototypical cortical circuit, aiding our understanding of neural function in both healthy and diseased brains.

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Suzuki, N., Tantirigama, M. L. S., Aung, K. P, Huang, H. H.-Y. & Bekkers, J. M. (2022) Fast and slow feedforward inhibitory circuits for cortical odor processing. eLife. 11: e73406, doi https://doi.org/10.7554/eLife.73406.

Potts, Y. & Bekkers, J. M. (2022) Dopamine increases the intrinsic excitability of parvalbumin-expressing fast-spiking cells in the piriform cortex. Front. Cell. Neurosci. 18: 919092, doi: 10.3389/fncel.2022.919092.

Bekkers, J. M. (2020)  Autaptic cultures: methods and applications.  Front. Synaptic Neurosci. 12, 18, doi 10.3389/fnsyn.2020.00018.

Ikeda, K., Suzuki, N. & Bekkers, J. M. (2018)  Sodium and potassium conductances in principal neurons of the mouse piriform cortex: A quantitative description.  J. Physiol. 596, 5397-5414.

Gerrard, L., Tantirigama, M. L. S. & Bekkers J. M. (2018)  Pre- and postsynaptic activation of GABAB receptors modulates principal cell excitation in the piriform cortex.  Front. Cell. Neurosci. 12, Article 28, 1-11.

Tantirigama, M. L. S., Huang, H. H.-Y. & Bekkers J. M. (2017)  Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding.  Proc. Natl. Acad. Sci. USA 114, 2407-2412.

Choy, J. M. C., Suzuki, N., Shima, Y., Budisantoso, T., Nelson, S. B., & Bekkers, J. M. (2017)  Optogenetic mapping of intracortical circuits originating from semilunar cells in the piriform cortex.  Cereb. Cortex 27, 589-601.

Suzuki, N., Tang, C. S.-M. & Bekkers, J. M. (2014)  Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity.  Front. Cell. Neurosci. 8, 76-86.

Bekkers, J. M. & Suzuki, N. (2013)  Neurons and circuits for odor processing in the piriform cortex.  Trends Neurosci. 36, 429-438.

Suzuki, N. & Bekkers, J. M. (2012)  Microcircuits mediating feedforward and feedback synaptic inhibition in the piriform cortex.  J. Neurosci. 32, 919-931.

Bekkers, J. M. (2011)  Changes in dendritic axial resistance alter synaptic integration in cerebellar Purkinje cells.  Biophys. J. 100, 1198-1206.

(Highlighted as a ‘Featured Article’, Biophys. J. 100, 2011.)

Suzuki, N. & Bekkers, J. M. (2011)  Two layers of synaptic processing by principal neurons in piriform cortex.  J. Neurosci. 31, 2156-2166.

(Highlighted in ‘This Week in the Journal’, J. Neurosci. 31, i, 2011.  Selected for Faculty of 1000 Biology as one of the top 2% of papers published in the biological sciences, based on the recommendations of >2000 of the world’s top researchers.)

Suzuki, N. & Bekkers, J. M. (2010)  Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex.  Cereb. Cortex 20, 2971-2984.

(Selected for front cover illustration.)

Suzuki, N. & Bekkers, J. M. (2010)  Inhibitory neurons in the anterior piriform cortex of the mouse: Classification using molecular markers.  J. Comp. Neurol. 518, 1670-1687.

Ikeda, K & Bekkers, J. M. (2009)  Two strategies for the efficient use of synaptic vesicles.  Commun. Integr. Biol. 2 (6), 1-4.

Ikeda, K. & Bekkers, J. M. (2009)  Counting the number of releasable synaptic vesicles in a presynaptic terminal. Proc. Natl. Acad. Sci. USA 106: 2945-2950.

Ikeda, K., Yanagawa, Y. & Bekkers, J. M. (2008)  Distinctive quantal properties of neurotransmission at excitatory and inhibitory autapses revealed using variance-mean analysis.  J. Neurosci. 28: 13563-13573.

(Selected for Faculty of 1000 Biology as one of the most interesting papers published in the biological sciences, based on the recommendations of >2000 of the world’s top researchers.)

Suzuki, N. & Bekkers, J. M. (2007)  Inhibitory interneurons in the piriform cortex.  Clin. Exp. Pharmacol. Physiol. 34, 1064-1069.

Bekkers, J. M. & Häusser, M. (2007)  Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output.  Proc. Natl. Acad. Sci. U.S.A. 104, 11447-11452.

Suzuki, N. & Bekkers, J. M. (2006)  Neural coding by two classes of principal cells in the mouse piriform cortex.  J. Neurosci. 26, 11938-11947.

(Subject of ‘Journal Club’ commentary in: Brann, J. H. et al. (2007), “Strategies for odor coding in the piriform cortex”.  J. Neurosci. 27, 1237-1238.)

McColl, C. D., Jacoby, A. S., Shine, J., Iismaa, T. P. & Bekkers, J. M. (2006) Galanin receptor-1 knockout mice exhibit spontaneous epilepsy, abnormal EEGs and altered inhibition in the hippocampus.  Neuropharmacol. 50, 209-218.

Bekkers, J. M. (2005)  Presynaptically-silent GABA synapses in hippocampus.  J. Neurosci. 25, 4031-4039.

Reid, C. A., Bekkers, J. M. & Clements, J. D. (2003)  Presynaptic Ca2+ channels: a functional patchwork.  Trends Neurosci. 26, 683-687.

Bekkers, J. M. (2003)  Convolution of mini distributions for fitting evoked synaptic amplitude histograms.  J. Neurosci. Meth. 130, 105-114.

Bekkers, J. M. & Delaney, A. J. (2001)  Modulation of excitability by a-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons.  J. Neurosci. 21, 6553-6560.

Chieng, B. & Bekkers, J. M. (2001)  Inhibition of calcium channels by opioid- and adenosine-receptor agonists in neurons of the nucleus accumbens.  Br. J. Pharmacol. 133, 337-344.

Bekkers, J. M. (2000)  Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large Layer 5 cortical pyramidal neurons of the rat.  J. Physiol. (Lond.) 525, 611-620.

(Commentary in: J. F. Storm, “K+ channels and their distribution in large cortical pyramidal neurones”, Perspectives, J. Physiol. (Lond.) 525, 565-566.)

Bekkers, J. M. (2000)  Properties of voltage-gated potassium currents in nucleated patches from large Layer 5 cortical pyramidal neurons of the rat.  J. Physiol. (Lond.) 525, 593-609.

Bekkers, J. M. (2000)  Distribution of slow AHP channels on hippocampal CA1 pyramidal neurons.  J. Neurophysiol. 83, 1756-1759.

Chieng, B. & Bekkers, J. M. (1999)  GABAB, opioid and  a2 receptor inhibition of calcium channels in acutely-dissociated locus coeruleus neurones.  Br. J. Pharmacol. 127, 1533-1538.

Bekkers, J. M. & Clements, J. D. (1999)  Quantal amplitude and quantal variance of strontium-induced asynchronous EPSCs in rat dentate granule neurons.  J. Physiol. (Lond.) 516, 227-248.  [Top 10 downloads from J. Physiol., April 2006.]

Reid, C. A., Bekkers, J. M. & Clements, J. D. (1998)  N-type and P/Q-type Ca2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal synapses.  J. Neurosci. 18, 2849-2855.

Clements, J. D. & Bekkers, J. M. (1997)  Detection of spontaneous synaptic events using an optimally scaled template.  Biophys. J. 73, 220-229.

Reid, C. A., Clements, J. D. & Bekkers, J. M. (1997)  Nonuniform distribution of Ca2+ channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures.  J. Neurosci. 17, 2738-2745.

Sah, P. & Bekkers, J. M. (1996)  Apical dendritic location of slow-afterhyperpolarization current in hippocampal pyramidal neurons: Implications for the integration of long-term potentiation.  J. Neurosci. 16, 4537-4542.

Bekkers, J. M., Vidovic, M. & Ymer, S. (1996)  Differential effects of histamine on the NMDA channel in hippocampal slices and cultures.  Neuroscience 72, 669-677.

Bekkers, J. M. & Stevens, C. F. (1996)  Cable properties of cultured hippocampal neurons determined from sucrose-evoked miniature EPSCs.  J. Neurophysiol. 75, 1250-1255.

Bekkers, J. M. & Stevens, C. F. (1995)  Quantal analysis of EPSCs recorded from small numbers of synapses in hippocampal cultures.  J. Neurophysiol. 73, 1145-1156.

Bekkers, J. M.  (1994)  Quantal analysis of synaptic transmission in the central nervous system, Curr. Opin. Neurobiol. 4, 360-365.

Bekkers, J. M. (1993)  Enhancement by histamine of NMDA-mediated synaptic transmission in the hippocampus.  Science  261, 104-106.

Bekkers, J. M. & Stevens, C. F. (1993)  NMDA receptors at excitatory synapses in the hippocampus: test of a theory of magnesium block.  Neurosci. Lett. 156, 73-77.

Keynes, R. D., Greeff, N. G., Forster, I. C. & Bekkers, J. M. (1991)  The effect of tetrodotoxin on the sodium gating current in the squid giant axon.  Proc. Roy. Soc. B 246, 135-140.

Bekkers, J. M. & Stevens, C. F. (1991)  Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture.  Proc. Natl. Acad. Sci. U.S.A. 88, 7834-7838.

Bekkers, J. M., Forster, I. C. & Greeff, N. G. (1990)  Gating current associated with inactivated states of the squid axon sodium channel.  Proc. Natl. Acad. Sci. U.S.A. 87, 8311-8315.

Bekkers, J. M. & Stevens, C. F. (1990)  Computational implications of NMDA receptor channels.  Cold Spring Harbor Symp. Quant. Biol. 55, 131-135.

Bekkers, J. M. & Stevens, C. F. (1990)  Presynaptic mechanism for long-term potentiation in the hippocampus.  Nature 346, 724-729.

(Commentary in: T. V. P. Bliss, “Maintenance is presynaptic”, News & Views, Nature 346, 698-699.)

Bekkers, J. M., Richerson, G. B. & Stevens, C. F. (1990)  Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices.  Proc. Natl. Acad. Sci. U.S.A. 87, 5359-5362.

Bekkers, J. M. & Stevens, C. F. (1989).  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus.  Nature 341, 230-233.

Bekkers, J. M., Greeff, N. G. & Keynes, R. D. (1986).  The conductance and density of sodium channels in the cut-open squid axon.  J. Physiol. (London) 377, 463-486.

Bekkers, J. M., Greeff, N. G., Keynes, R. D. & Neumcke, B. (1984).  The effect of local anaesthetics on the components of the asymmetry current in the squid giant axon.  J. Physiol. (London) 352, 653-668.

Invited Commentaries and Book Chapters

Australian Brain Alliance* (2019)  A neuroethics framework for the Australian Brain Initiative.  Neuron 101, 365-369. * Co-author: Bekkers, J. M., member of Australian Brain Alliance Steering Committee.

Bekkers, J. M. (2013)  Axial resistivity.  In Encyclopedia of Computational Neuroscience, Jaeger, D. & Jung, R. (eds) SpringerReference (SpringerReference.com), Springer-Verlag, Berlin & Heidelberg.

Bekkers, J. M. (2011)  Quick guide: Pyramidal cells.  Curr. Biol. 21, R975.

Daria, V. R., Stricker, C., Bekkers, J. M., Redman, S. J. & Bachor, H. A. (2010)  Dynamic complex optical fields for optical manipulation, 3D microscopy, and photostimulation of neurotransmitters.  In Proc. SPIE Optical Trapping and Optical Micromanipulation VII, Dholakia, K. & Spalding, G. C. (eds), Vol 7762, Article No. 77621S.

Bekkers, J. M. (2009) Excitatory autapses find a function?  Curr. Biol. 19, R296-R298.

Ikeda, K. & Bekkers, J. M. (2006)  Quick guide: Autapses.  Curr. Biol. 16, R308.

Richerson, G. B. & Bekkers, J. M. (2004)  Learning to take a deep breath – with BDNF.  Nature Med. 10, 25-26.

Bekkers, J. M. (2003)  Functional autapses in the cortex.  Curr. Biol 13, R433-R435.

Bekkers, J. M. (2002)  A new kind of inhibition.  Curr. Biol 12, R648-R650.

Bekkers, J. M. (2000)  MultiClamp 700A Computer-Controlled Current- and Voltage-Clamp Amplifier: Theory and Operation.  Axon Instruments, Inc., 138 pp.

Bekkers, J. M. (1998)  Are autapses prodigal synapses?  Curr. Biol. 8, R52-R55.

Bekkers, J. M. (1998)  Strontium-evoked mEPSCs reveal large quantal variance at central glutamate synapses.  In Central synapses: quantal mechanisms and plasticity, D. Faber, H. Atwood, H. Korn, S. Redman, S. Thomson & J. Altman (eds) (HFSP, Strasbourg), pp 115-123.

Bekkers, J. M. (1998)  Sucking up to cells: The patch clamp technique in neuroscience.  In A Beginner’s Guide to Neuroscience Methods, R. L. Martin (ed) (Harwood Academic Press, Amsterdam), pp 40-45.

Bekkers, J. M. (1998)  The brain in a dish: How to study acutely dissociated and cultured neurons.  In A Beginner’s Guide to Neuroscience Methods, R. L. Martin (ed) (Harwood Academic Press, Amsterdam), pp 11-16.

Bekkers, J. M. & Stevens, C. F. (1994)  The nature of quantal transmission at central excitatory synapses.  In Cellular and Molecular Mechanisms of Transmitter Release, L. Stjarne (ed) (Raven Press) 261-273.

Bekkers, J. M. (1993)  The laboratory setup.  In The Axon Guide for Electrophysiology & Biophysics Laboratory Techniques, R. Sherman-Gold (ed) (Axon Instruments, Foster City, California) pp 17-24.

Bekkers, J. M. & Stevens, C. F. (1992)  Osmotic stimulation of presynaptic terminals.  In Electrophysiological Methods for In Vitro Studies in Vertebrate Neurobiology, H. Kettenmann & R. Grantyn (eds) (Wiley-Liss, New York), pp 150-154; and front cover.

Bekkers, J. M. & Stevens, C. F. (1991)  Application of quantal analysis to the study of long-term potentiation: errors, assumptions and precautions.  In Long-Term Potentiation: A Debate of Current Issues, M. Baudry & J. Davis (eds) (MIT Press) pp 63-76.

Bekkers, J. M. & Stevens, C. F. (1990).  Two different ways evolution makes neurons larger.  In Understanding the Brain through the Hippocampus: The Hippocampal Region as a Model for Studying Brain Structure and Function. (eds Storm-Mathisen, J., Zimmer, J. & Ottersen, O. P.) pp 37-45 (Elsevier, Amsterdam).

Bekkers, J. M. & Stevens, C. F. (1989).  Dual modes of excitatory synaptic transmission in the brain.  In Molecular Neurobiology.  Proceedings of the First NIMH Conference. (eds Zalcman, S., & Scheller, R.) (U.S. Department of Health and Human Services, National Institute of Mental Health) pp 39-50.

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