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Biol. Bull. 201: 276-277. (October 2001)
© 2001 Marine Biological Laboratory

Cholinergic Modulation of Odor-Evoked Oscillations in the Frog Olfactory Bulb

Benjamin Hall and Kerry Delaney1

Marine Biological Laboratory, Woods Hole, Massachusetts 02543

The vertebrate olfactory bulb (OB) receives sensory information from peripheral odorant receptors and transmits this information to other cortical regions. OB output is encoded in the spiking patterns of the primary OB neurons—the mitral and tufted mitral cells (MTCs)—which project directly to higher cortical centers. The activity of the MTCs is determined both by patterns of odorant receptor activation and by interactions with intrinsic inhibitory interneurons within the OB. OB output is thus shaped by the two major classes of interneurons: the periglomerular cells (PGs) and the granule cells (GCs). GCs make distributed reciprocal dendrodendritic synaptic contacts along the secondary dendrites of MTCs and, via GABA release, provide both feedback and feedforward inhibition of the primary neurons (1). In addition, these reciprocal circuits are thought to be the site of generation of odor-evoked oscillations in the OB. In vertebrates, including frogs, GC dendrites receive prominent cholinergic innervation from the basal forebrain, mediated in the GC layer by muscarinic acetylcholine (mACh) receptors (2). Although studies have investigated the effects of ACh modulation in the OB in response to nerve activation and at the MTC to GC synapse in slice preparations, the effect of mACh agonists on natural odorant-evoked oscillations in the OB is unknown (3,4).

We examined odor-evoked oscillatory responses in the frog olfactory bulb using an in vitro nose and brain preparation, in which we can maintain intact the olfactory circuitry from nose to cortex (5). We bath-applied the mACh agonist oxotremorine and monitored local field potential (LFP) electrodes placed in the external plexiform layer of the OB to examine the effect of this mACh agonist on odor-evoked activity.

Airborne odorants were delivered to the exposed nares (within {approx}3 mm) by means of electrically controlled pressure pulses (0.5 psi–1.5 psi/50–300 ms) that introduced a pulse of clean charcoal-filtered air through a saturated odorized volume (amyl acetate) or via addition of an odorized bolus into a continuous clean airstream. Oxotremorine (sesquifumarate salt) was mixed fresh daily in regular Ringer’s solution and bath-applied at 100 µM. Bicuculline was aliquoted in distilled water and diluted (1000-fold) in Ringer’s to 10 µM.

Odor-evoked oscillations in the frog OB, recorded in the external plexiform layer, consisted of an initial biphasic component (0–300 ms) followed by a slow wave envelope (1 to 2 s in duration) and a superimposed fast oscillation ({approx}7–12 Hz) (Fig. 1A). The parameters of the odor-evoked response are consistent with our previous observations and similar to observations in turtle OB (5,6). The fast oscillation was completely and reversibly blocked by bath application of the GABAA antagonist bicuculline (10 µM), demonstrating that GABAA inhibition is required to maintain these oscillations (data not shown). Analysis of LFP recordings determined that oxotremorine had two distinct effects on the OB LFP response. First, it enhanced the initial component (0–300 ms) of the olfactory response by {approx}25% (126.6 ± 4.2%; mean ± SE; n = 16 trials in four animals; P < 0.001) (Fig. 1B); second, it increased the power of the frequency spectrum of LFP recordings between 2 and 10 Hz by 75% (175.2 ± 8.1%; mean ± SE; n = 16 trials in four animals) (Fig. 1C).



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  		Figure 1. Effects of the muscarinic acetylcholine (mACh) receptor agonist oxotremorine (100 µM) on the odor-evoked local field potential (LFP) response in frog olfactory bulb. (A) The characteristic response to odor application at the nose (200 ms-bar) was an initial, typically biphasic, component followed by a slow wave and superimposed fast (7–12 Hz) oscillations. (B) Bath application of the mACh agonist increased the peak amplitude of the initial component (* in A). (C) Power spectral density analysis of the LFP showed increased power in the presence of the mACh agonist between 2 and 10 Hz. Inset in C shows representative averages of three single traces in each condition showing the fast oscillation high-pass filtered to 3.5 Hz (scale bar as in A).

 
In conclusion, the in vitro preparation of frog nose and brain is a system which, by offering access for stimulating electrodes to the forebrain nuclei from which these fibers arise, permits us to study the effects of centrifugal ACh release in the OB. Our data here, showing enhancement of the LFP in the OB, predict that mACh receptor activation may improve the spatial coherence of OB activity. We speculate that one function for this mACh modulation may be to drive synchrony of the OB output necessary for plasticity at the level of lateral (olfactory) cortex.

This project was generously supported by the Grass Foundation and by the Canadian Institutes of Health Research. BH would like to thank all of the Grass Fellows and Kim Hoke and Melissa Vollrath for their comments on the manuscript.

Footnotes

1 Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6. Back

Literature Cited

  1. Shepherd, G. M., and C. A. Greer. 1990. Pp. 133–169 in The Synaptic Organization of the Brain, G. M. Shepherd, ed., Oxford University Press, New York.
  2. Crespo, C., J. M. Blasco-Ibanez, J. G. Brinon, J. R. Alonso, M. I. Dominquez, and F. J. Martinez-Guijarro. 2000. Eur. J. Neurosci., 12(11): 3963–3974.[ISI][Medline]
  3. Castillo, P. E., A. Carleton, J. D. Vincent, and P. M. Lledo. 1999. J. Neurosci., 19(21): 9180–9191.[Abstract/Free Full Text]
  4. Elaagouby, A., N. Ravel, and R. Gervais. 1991. Neuroscience, 45(3): 653–662.[ISI][Medline]
  5. Delaney, K. R., and B. J. Hall. 1996. J. Neurosci. Methods, 68(2): 193–202.[ISI][Medline]
  6. Lam, Y. W., L. B. Cohen, M. Wachowiak, and M. R. Zochowski. 2000. J. Neurosci., 20(2): 749–762.[Abstract/Free Full Text]



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