Synchronous Bursting among Juxtaglomerular Neurons

Summary

Principal Investigator: ABDALLAH M HAYAR
Abstract: Oscillations, bursting, and resonance have been linked to synchronization of neuronal activity and to the emergence of brain rhythms. Using simultaneous whole-cell recording from pairs of juxtaglomerular (JG) olfactory bulb neurons, we were the first to discover that membrane potential oscillations and spontaneous bursting activity are highly correlated in external tufted (ET) cells associated with the same glomeruli. This synchronous activity occurs at theta frequency (2-7 Hz), the same frequency that characterizes investigative sniffing in rodents. Synchronous ET cell bursting may play an important role in olfactory coding and in regulating the induction of synaptic plasticity at the first input stage of the main olfactory bulb. We have further found that synchronous activity among bursting neurons persists in the presence of blockers of fast glutamatergic and GABAergic synaptic transmission. These findings suggest that synchrony could be mediated by slowly acting neurotransmitters and/or by non-synaptic interactions such as gap junctions that interconnect ET cells. Synchronously active ET cells could, in turn, via synaptic interactions synchronize other JG neurons, as well as mitral cells, the major output neurons of the olfactory bulb. This project will assess the functional roles of synaptic and non-synaptic interactions in establishing synchronous activity among electrophysiologically and morphologically characterized JG neurons. Further, it will investigate the functional significance of synchronous bursting by analyzing short-term facilitation of excitatory postsynaptic potentials that are evoked by ET cell bursts in periglomerular and short axon cells of the same glomerulus. This would support the idea that glomerular interneurons that are postsynaptic to ET cells, may act as coincident input detectors, firing optimally upon receiving synchronous bursting input. Taken together, these experiments will provide important, new insight into the intrinsic synaptic organization of the glomeruli and the role of glomerular circuitry in olfactory coding.
Funding Period: 2004-05-01 - 2009-04-30
more information: NIH RePORT

Top Publications

  1. pmc Properties of external plexiform layer interneurons in mouse olfactory bulb slices
    K A Hamilton
    Department of Cellular Biology and Anatomy, Louisiana State University Health Sciences Center, 1501 Kings Highway, Shreveport, LA 71130 3932, USA
    Neuroscience 133:819-29. 2005
  2. pmc Cholinergic modulation of GABAergic and glutamatergic transmission in the dorsal subcoeruleus: mechanisms for REM sleep control
    David S Heister
    Center for Translational Neuroscience, Department of Neurobiology and Developmental Sciences, University ofArkansas for Medical Sciences, Little Rock, AR 72205, USA
    Sleep 32:1135-47. 2009
  3. pmc Metabotropic glutamate receptors and dendrodendritic synapses in the main olfactory bulb
    Hong Wei Dong
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA
    Ann N Y Acad Sci 1170:224-38. 2009
  4. pmc Noradrenergic regulation of GABAergic inhibition of main olfactory bulb mitral cells varies as a function of concentration and receptor subtype
    Qiang Nai
    Dept of Anatomy, Univ of Tennessee Health Science Ctr, 855 Monroe Ave, Suite 515, Memphis, TN 38163, USA
    J Neurophysiol 101:2472-84. 2009
  5. pmc An improved method for patch clamp recording and calcium imaging of neurons in the intact dorsal root ganglion in rats
    Abdallah Hayar
    Center for Translational Neuroscience, Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, AR, United States
    J Neurosci Methods 173:74-82. 2008
  6. pmc Electrical coupling: novel mechanism for sleep-wake control
    Edgar Garcia-Rill
    Center for Translational Neuroscience, Department of Neurobiology and Dev Sci, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA
    Sleep 30:1405-14. 2007
  7. pmc Activation of postsynaptic GABAB receptors modulates the bursting pattern and synaptic activity of olfactory bulb juxtaglomerular neurons
    Nikolay Karpuk
    Deptepartment of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205, USA
    J Neurophysiol 99:308-19. 2008
  8. pmc Endogenous GABA and glutamate finely tune the bursting of olfactory bulb external tufted cells
    Abdallah Hayar
    Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205, USA
    J Neurophysiol 98:1052-6. 2007
  9. pmc Activation of group I metabotropic glutamate receptors on main olfactory bulb granule cells and periglomerular cells enhances synaptic inhibition of mitral cells
    Hong Wei Dong
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA
    J Neurosci 27:5654-63. 2007
  10. pmc Evidence for Electrical Coupling in the SubCoeruleus (SubC) Nucleus
    David S Heister
    Center for Translational Neuroscience, Dept of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, 4301 W Markham St, Slot 847, Little Rock, AR 72205, USA
    J Neurophysiol 97:3142-7. 2007

Scientific Experts

Detail Information

Publications15

  1. pmc Properties of external plexiform layer interneurons in mouse olfactory bulb slices
    K A Hamilton
    Department of Cellular Biology and Anatomy, Louisiana State University Health Sciences Center, 1501 Kings Highway, Shreveport, LA 71130 3932, USA
    Neuroscience 133:819-29. 2005
    ..Together, these results suggest that EPL interneurons are excited by M/T cells via AMPA/kainate receptors and may in turn inhibit M/T cells within spatial domains that are topographically related to several adjacent glomeruli...
  2. pmc Cholinergic modulation of GABAergic and glutamatergic transmission in the dorsal subcoeruleus: mechanisms for REM sleep control
    David S Heister
    Center for Translational Neuroscience, Department of Neurobiology and Developmental Sciences, University ofArkansas for Medical Sciences, Little Rock, AR 72205, USA
    Sleep 32:1135-47. 2009
    ....
  3. pmc Metabotropic glutamate receptors and dendrodendritic synapses in the main olfactory bulb
    Hong Wei Dong
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA
    Ann N Y Acad Sci 1170:224-38. 2009
    ..This chapter focuses on recent advances in our understanding of mGluR-mediated signaling components at dendrodendritic synapses...
  4. pmc Noradrenergic regulation of GABAergic inhibition of main olfactory bulb mitral cells varies as a function of concentration and receptor subtype
    Qiang Nai
    Dept of Anatomy, Univ of Tennessee Health Science Ctr, 855 Monroe Ave, Suite 515, Memphis, TN 38163, USA
    J Neurophysiol 101:2472-84. 2009
    ....
  5. pmc An improved method for patch clamp recording and calcium imaging of neurons in the intact dorsal root ganglion in rats
    Abdallah Hayar
    Center for Translational Neuroscience, Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, AR, United States
    J Neurosci Methods 173:74-82. 2008
    ....
  6. pmc Electrical coupling: novel mechanism for sleep-wake control
    Edgar Garcia-Rill
    Center for Translational Neuroscience, Department of Neurobiology and Dev Sci, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA
    Sleep 30:1405-14. 2007
    ....
  7. pmc Activation of postsynaptic GABAB receptors modulates the bursting pattern and synaptic activity of olfactory bulb juxtaglomerular neurons
    Nikolay Karpuk
    Deptepartment of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205, USA
    J Neurophysiol 99:308-19. 2008
    ..Thus the postsynaptic GABA(B)-Rs on ET cells may play an important role in shaping the activation pattern of the glomeruli during olfactory coding...
  8. pmc Endogenous GABA and glutamate finely tune the bursting of olfactory bulb external tufted cells
    Abdallah Hayar
    Department of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205, USA
    J Neurophysiol 98:1052-6. 2007
    ..We suggest that ET cell excitatory and inhibitory inputs may be encoded as a change in the pattern of spike bursting in ET cells, which together with mitral/tufted cells constitute the output circuit of the olfactory bulb...
  9. pmc Activation of group I metabotropic glutamate receptors on main olfactory bulb granule cells and periglomerular cells enhances synaptic inhibition of mitral cells
    Hong Wei Dong
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA
    J Neurosci 27:5654-63. 2007
    ..We speculate that mGluRs amplify spike-driven lateral inhibition through the mitral-to-granule cell circuit, whereas GL mGluRs may play a more important role in amplifying intraglomerular inhibition after subthreshold input...
  10. pmc Evidence for Electrical Coupling in the SubCoeruleus (SubC) Nucleus
    David S Heister
    Center for Translational Neuroscience, Dept of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, 4301 W Markham St, Slot 847, Little Rock, AR 72205, USA
    J Neurophysiol 97:3142-7. 2007
    ..The presence of electrical coupling in the SubC introduces a novel potential mechanism of action for the regulation of sleep-wake states...
  11. pmc Spontaneous field potentials in the glomeruli of the olfactory bulb: the leading role of juxtaglomerular cells
    S V Karnup
    University of Maryland Medical School, Department of Physiology, 655 West Baltimore Street, Baltimore, MD 21201 1559, USA
    Neuroscience 142:203-21. 2006
    ..Finally, we hypothesize that the GL is not a set of independent modules, but it represents a subsystem in the MOB network, which can perform initial processing of odors...
  12. pmc Olfactory nerve-evoked, metabotropic glutamate receptor-mediated synaptic responses in rat olfactory bulb mitral cells
    Matthew Ennis
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, TN 38163, USA
    J Neurophysiol 95:2233-41. 2006
    ....
  13. pmc A low-cost solution to measure mouse licking in an electrophysiological setup with a standard analog-to-digital converter
    Abdallah Hayar
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, 855 Monroe Avenue, Suite 515, Memphis, TN 38163, USA
    J Neurosci Methods 153:203-7. 2006
    ..This method does not produce any significant electrical artifacts and can be combined with electrophysiological measurements of single unit activity from neurons involved in the control of the licking behavior...
  14. pmc Olfactory bulb external tufted cells are synchronized by multiple intraglomerular mechanisms
    Abdallah Hayar
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, USA
    J Neurosci 25:8197-208. 2005
    ..These findings suggest that coordinated synaptic transmission and gap junction coupling synchronize the spontaneous bursting of ET cells of the same glomerulus...
  15. pmc Group I mGluR activation enhances Ca(2+)-dependent nonselective cation currents and rhythmic bursting in main olfactory bulb external tufted cells
    Hong Wei Dong
    Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, 38163, USA
    J Neurosci 29:11943-53. 2009
    ....