Elsevier

Experimental Neurology

Volume 14, Issue 1, January 1966, Pages 44-56
Experimental Neurology

Dendrodendritic synaptic pathway for inhibition in the olfactory bulb

https://doi.org/10.1016/0014-4886(66)90023-9Get rights and content

Abstract

Anatomical and physiological evidence based on independent studies of the mammalian olfactory bulb points to synaptic interactions between dendrites. A theoretical analysis of electric potentials in the rabbit olfactory bulb led originally to the conclusion that mitral dendrites synaptically excite granule dendrites and granule dendrites then synaptically inhibit mitral dendrites. In an independent electron micrographic study of the rat olfactory bulb, synaptic contacts were found between granule and mitral dendrites. An unusual feature was the occurrence of more than one synaptic contact per single granule ending on a mitral dendrite; as inferred from the morphology of these synaptic contacts, a single granule ending was often presynaptic at one point and postsynaptic at an adjacent point with respect to the contiguous mitral dendrite. We postulate that these synaptic contacts mediate mitral-to-granule excitation and granule-to-mitral inhibition. These dendrodendritic synapses could provide a pathway for both lateral and self inhibition.

References (26)

  • W. Rall

    Electrophysiology of a dendritic neuron model

    Biophys. J.

    (1962)
  • R. Von Baumgarten et al.

    Slow waves in the olfactory bulb and their relation to unitary discharges

    Electroencephalog. Clin. Neurophysiol.

    (1962)
  • K.H. Andres

    Der Feinbau des Bulbus olfactorius der Ratte unter besonderer Berücksichtigung der synaptischen Verbindindungen

    Z. Zellforsch. Mikroskop. Anat.

    (1965)
  • J. Castillo et al.

    Changes in end-plate activity produced by pre-synaptic polarization

    J. Physiol. London

    (1954)
  • M. Colonnier et al.

    Synaptic organization in the lateral geniculate nucleus of the monkey

    Z. Zellforsch. Mikroskop. Anat.

    (1965)
  • K.B. Doving

    Studies of the relation between the frog's electro-olfactogram (EOG) and single unit activity in the olfactory bulb

    Acta Physiol. Scand.

    (1964)
  • J. Dowling et al.

    Organization of the primate retina

  • E.G. Gray

    Axo-somatic and axo-dendritic synapses of the central cortex; an electron microscopic study

    J. Anat.

    (1959)
  • E.G. Gray

    A morphological basis for pre-synaptic inhibition?

    Nature

    (1962)
  • H.K. Hartline et al.

    Inhibition in the eye of Limulus

    J. Gen. Physiol.

    (1956)
  • Y. Hirata

    Some observations on the fine structure of the synapses in the olfactory bulb of the mouse, with particular reference to the atypical synaptic configuration

    Arch. Histol. Okayama [Saibo Kaku Byorigaku Zasshi]

    (1964)
  • M. Kidd

    Electron microscopy of the inner plexiform layer of the retina in the cat and pigeon

    J. Anat.

    (1962)
  • A.W. Liley

    The effects of presynaptic polarization on the spontaneous activity at the mammalian neuromuscular junction

    J. Physiol. London

    (1956)
  • Cited by (520)

    • Postsynaptic activity of inhibitory neurons evokes hemodynamic fMRI responses: GABAergic neurons initiate functional hyperemia

      2021, NeuroImage
      Citation Excerpt :

      Specifically, the apical dendrites of GABAergic granule cells connect to the lateral dendrites of excitatory mitral (and tufted) cells in the external plexiform layer (EPL) via reciprocal dendrodendritic synapses (Bartel et al., 2015; Price and Powell, 1970; Rall and Shepherd, 1968), which mediate lateral inhibition and regulate excitatory spread along mitral cell dendrites (Luo and Katz, 2001; Xiong and Chen, 2002; Yokoi et al., 1995). Importantly, preferential activation of these inhibitory neurons has been shown with antidromic stimulation of the lateral olfactory tract (LOT), which contain the mitral cell axons (Jahr and Nicoll, 1980; Mori and Takagi, 1978; Rall et al., 1966). Local field potentials (LFPs) evoked by LOT stimulation have a signature waveform indicating the excitation of inhibitory granule cells (Nakashima et al., 1978; Nicoll, 1969; Uva et al., 2006), and current source density analyses of laminar LFPs revealed a localized current sink (i.e. synaptic depolarization) in EPL (Aroniadou-Anderjaska et al., 1999; Poplawsky et al., 2015; Uva et al., 2006).

    View all citing articles on Scopus
    1

    Figures 1 and 3 were drawn by Mrs. G. Turner.

    View full text