Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Making Scents Out of Spatial and Temporal Codes in Specialist and Generalist Olfactory Networks
ARL Division of Neurobiology, University of Arizona, Tucson, AZ 85721, USA
Correspondence to be sent to: Thomas A. Christensen, e-mail: tc{at}neurobio.arizona.edu
Key words: lateral inhibition, odor coding, olfactory glomeruli, oscillations, synchronization
 |
Introduction |
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 Top Introduction Heterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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The first-order olfactory centers in the brains of vertebrates and invertebrates are characterized by arrays of morphologically discrete glomeruli, and cross-phyletic comparisons have repeatedly found striking similarities in glomerular organization across evolutionarily remote animals. A growing list of studies shows that the vertebrate olfactory bulb (OB) and insect antennal lobe (AL) are organized chemotopically, and an individual glomerulus reflects the odor-response profile of the olfactory receptor neurons (ORNs) that converge on it (Bozza and Kauer, 1998
;
Belluscio et al., 2002;
Ng et al., 2002;
Wang et al., 2003). While
these different studies using a wide range of methods have supported glomerular chemotopy
in diverse species, many fundamental questions about the neural circuitry underlying
these activity patterns remain. Evidence is increasing, in fact, that the molecular
receptive range (MRR) or ‘odor tuning’ of a glomerulus is also shaped by
interglomerular—and particularly inhibitory—interactions (Christensen et al., 1998;
Lei et al., 2002;
Sachse and Galizia, 2003;
Aungst et al., 2003;
Nagayama et al., 2004), but
the cellular and synaptic mechanisms underlying this modulation remain poorly
understood. |
Heterogeneity in glomerular output |
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TopIntroductionHeterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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While uniglomerular projection neurons (PNs) associated with a given glomerulus have similar MRRs, mitral and tufted (M/T) cells in mammals (Nagayama et al., 2004
) and the diverse PNs that
innervate the same glomerulus in insects (Vickers
et al., 1998;
Sadek et al., 2002) have
been shown to differ in their physiological responses to odors. These findings emphasize
that glomeruli are not isolated ‘islands’ of neuropil or simple relay
elements, and an increasing number of studies, many in insects, show that the MRR and/or
dynamics of a PN’s odor-evoked response are influenced by interactions with other
glomeruli. For instance, interglomerular AL circuitry in both honey bees (Sachse and Galizia, 2003) and moths (Vickers et al., 1998;
Lei et al., 2002) can modify
the relatively narrow tuning of the ORNs that provide input to a glomerulus, resulting in
a modification of PN responses. This is especially evident when the blend of odors that
selectively activates several identified glomeruli simultaneously is used as a stimulus
(Christensen et al., 2000;
Christensen and Hildebrand, 2002). The
same may not be true, however, for glomeruli in the fruit fly Drosophila. In a
recent study using electrophysiological recordings, it was proposed that network
mechanisms can transform the odor tuning of glomerular outputs (Wilson et al., 2004), while two other studies
using activity labeling failed to find any such signal transformation (Ng et al., 2002;
Wang et al., 2003). Reasons
for such divergent results remain unclear, emphasizing the need to learn more about the
complex synaptic circuitry in the glomerular neuropil. |
‘Specialists’ versus ‘generalists’ |
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TopIntroductionHeterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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Recent studies in a variety of insect species have provided compelling evidence that receptor cells previously identified as ‘generalists’ (e.g. responding to multiple plant-derived volatiles) exhibit much greater selectivity and sensitivity when stimulated with the appropriate odor ligand (Ignell and Hansson, 2004
;
Skiri et al., 2004). This is
true also at the central level. We recently found glomeruli that are very selective for
enantiomers of a plant monoterpene (Reisenman
et al., 2004) and another that is extremely sensitive to
CO2 (Guerenstein et al.,
2004). It seems, therefore, that the sometimes false characterization of
olfactory receptors and central neurons as ‘broadly tuned’ may be due to the
lack of a well-defined key stimulus and/or the use of unnaturally elevated odor
concentrations (Christensen and Hildebrand,
2002;
Ignell and Hansson, 2004). Since odor
selectivity and sensitivity are inextricably linked, care should be exercised in
characterizing any olfactory cells or networks as ‘specialists’ or
‘generalists’ unless a sufficient number of odors are tested using a
physiologically appropriate range of concentrations. |
Synchrony with and without oscillations |
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TopIntroductionHeterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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The brain’s information coding strategies have been debated for many years, and this discussion has included the mechanisms by which odors are discriminated. Since the 1940s, when Adrian first recorded from the OB, a number of investigators have found evidence for a possible functional role of oscillatory activity in odor coding (Adrian, 1942
;
Gelperin et al., 1996;
Kashiwadani et al., 1999;
Laurent et al., 2001;
Friedrich, 2002), but this remains an
area of active debate, at both the physiological and behavioral levels. In the locust and
honeybee, for example, studies suggest that network oscillations may be important for
encoding olfactory information (reviewed in
Laurent et al., 2001),
whereas studies in moths have not been able to substantiate these findings (Christensen et al., 1998, 2000, 2003;
Heinbockel et al., 1998;
Vickers et al., 1998, 2001;
Daly et al., 2004a). Aside
from species differences, such divergent findings may also result from our lack of
detailed knowledge about the synaptic circuitry that encodes olfactory information in the
OB and AL. Another possibility is that most published experimental-stimulus protocols
have not addressed whether oscillatory patterning is maintained under conditions that
mimic natural odor plumes (Vickers et
al., 2001;
Ditzen et al., 2003;
Uchida and Mainen, 2003). Yet another
possible source of disagreement may reflect the fundamental ability of sensory circuits
in the brain to be modulated by experience, as we recently demonstrated in
Manduca (Daly et al.,
2004b). In sum, recent findings challenge the idea that specific, slow
temporal patterns of activity encode different odors. Instead, they support numerous
studies in both invertebrates and vertebrates arguing that much of the information
encoded in spiking patterns in sensory systems is associated with stimulus dynamics
(Buraças and Albright, 1999)
and that these patterns can be modified by learning (Wilson and Stevenson, 2003). Future studies that seek to
understand olfactory coding from the animal’s perspective will no doubt lead to new
revelations about the functional significance of temporally patterned neural activity as
it relates to the natural dynamics of odor plumes. |
Acknowledgements |
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TopIntroductionHeterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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Many thanks to the talented folks in John Hildebrand’s lab who have contributed to this work, especially Andrew Dacks, Pablo Guerenstein, Hong Lei, Vince Pawlowski, Carolina Reisenman and Heather Stein. This work is supported by National Institute on Deafness and Other Communication Disorders Grants DC-05652 to T.A.C. and DC-02751 to J.G.H.
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References |
|---|
|
TopIntroductionHeterogeneity in glomerular...‘Specialists’ versus...Synchrony with and without...AcknowledgementsReferences |
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Adrian, E.D. (1942) Olfactory reactions in the brain of the hedgehog. J. Physiol., 100, 459–473.
Aungst, J., Heyward, P., Puche, A., Karnup, S., Hayar, A., Szabo, G. and Shipley, M. (2003) Centre–surround inhibition among olfactory bulb glomeruli. Nature, 426, 623–629.[CrossRef][Medline]
Belluscio, L., Lodovichi, C., Feinstein, P., Mombaerts, P. and Katz, L.C. (2002) Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature, 419, 296–300.[CrossRef][Medline]
Bozza, T.C. and Kauer, J.S. (1998) Odorant response properties of convergent olfactory receptor neurons. J. Neurosci., 18, 4560–4569.
Buraças, G.T. and Albright, T.D. (1999) Gauging sensory representations in the brain. Trends Neurosci., 22, 303–309.[CrossRef][ISI][Medline]
Christensen, T.A. and Hildebrand, J.G. (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr. Opin. Neurobiol., 12, 393–399.[CrossRef][ISI][Medline]
Christensen, T.A., Waldrop, B.R. and Hildebrand, J.G. (1998) Multitasking in the olfactory system: context-dependent resonses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J. Neurosci., 18, 5999–6008.
Christensen, T.A., Pawlowski, V.M., Lei, H. and Hildebrand, J.G. (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific ensembles. Nat. Neurosci., 3, 927–931.[CrossRef][ISI][Medline]
Christensen, T.A., Lei, H. and Hildebrand, J.G. (2003) Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons. Proc. Natl Acad. Sci. USA, 100, 11076–11081.
Daly, K.C., Wright, G.A. and Smith, B.H. (2004a) Molecular features of odorants systematically influence slow temporal responses across clusters of coordinated antennal lobe units in the moth Manduca sexta. J. Neurophysiol., 92, 236–254.
Daly, K.C., Christensen, T.A., Lei, H., Smith, B.H. and Hildebrand, J.G. (2004b) Learning modulates the ensemble representations for odors in primary olfactory networks. Proc. Natl Acad. Sci. USA, 101, 10476–10481.
Ditzen, M., Ever, J.-F. and Galizia, C.G. (2003) Odor similarity does not influence the time needed for odor processing. Chem. Senses, 28, 781–789.
Friedrich, R.W. (2002) Real time odor representations. Trends Neurosci., 25, 487–489.[CrossRef][ISI][Medline]
Gelperin, A., Kleinfeld, D., Denk, W. and Cooke, I.R.C. (1996) Oscillations and gaseous oxides in invertebrate olfaction. J. Neurobiol., 30, 110 –122.[CrossRef][ISI][Medline]
Guerenstein, P., Christensen, T.A. and Hildebrand, J.G. (2004) Sensory processing of ambient-CO2 information in the brain of the moth Manduca sexta. J. Comp. Physiol. A, 190, 707–725.
Heinbockel, T., Kloppenburg, P. and Hildebrand, J.G. (1998) Pheromone-evoked potential and oscillations in the antennal lobes of the sphinx moth Manduca sexta. J. Comp. Physiol. A, 182, 703–714.
Ignell, R. and Hansson, B.S. (2004) Insect olfactory neuroethology—an electrophysiological perspective. In Christensen, T.A. (ed), Advances in Insect Sensory Neuroscience. CRC Press, Boca Raton, FL, in press.
Kashiwadani, H., Sasaki, Y.F., Uchida, N. and Mori, K. (1999) Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J. Neurophysiol., 82, 1786–1792.
Laurent, G., Stopfer, M., Friedrich, R.W., Rabinovich, M.I., Volkovskii, A. and Abarbanel, H.D.I. (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci., 24, 263–297.[CrossRef][ISI][Medline]
Lei, H., Christensen, T.A. and Hildebrand, J.G. (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat. Neurosci., 5, 557–565.[CrossRef][ISI][Medline]
Nagayama, S., Takahashi, Y.K., Yoshihara, Y. and Mori, K. (2004) Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J. Neurophysiol., 91, 2532–2540.
Ng, M., Roorda, R.D., Lima, S.Q., Zemelman, B.V., Morcillo, P. and Miesenbock, G. (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron, 36, 463–474.[CrossRef][ISI][Medline]
Reisenman, C.E., Christensen, T.A., Francke, W. and Hildebrand, J.G. (2004) Enantioselectivity of projection neurons innervating identified olfactory glomeruli. J. Neurosci., 24, 2602–2611.
Sachse, S. and Galizia, C.G. (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur. J. Neurosci., 18, 2119–2132.[CrossRef][ISI][Medline]
Sadek, M.M., Hansson, B.S., Rospars, J.P. and Anton, S. (2002) Glomerular representation of plant volatiles and sex pheromones components in the antennal lobe of the female Spodoptera littoralis. J. Exp. Biol., 205, 1363–1376.
Skiri, H.T., Galizia, C.G. and Mustaparta, H. (2004) Representation of primary plant odorants in the antennal lobe of the moth Heliothis virescens using calcium imaging. Chem. Senses, 29, 253–267.
Uchida, N. and Mainen, Z.F. (2003) Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci., 6, 1224–1229.[CrossRef][ISI][Medline]
Vickers, N.J., Christensen, T.A. and Hildebrand, J.G. (1998) Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol., 400, 35–56.[CrossRef][ISI][Medline]
Vickers, N.J., Christensen, T.A., Baker, T.C. and Hildebrand, J.G. (2001) Odour-plume dynamics influence the brain’s olfactory code. Nature, 410, 466–470.[CrossRef][Medline]
Wang, J.W., Wong, A.M., Flores, J., Vosshall, L.B. and Axel, R. (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 112, 271–282.[CrossRef][ISI][Medline]
Wilson, D.A. and Stevenson, R.J. (2003) The fundamental role of memory in olfactory perception. Trends Neurosci., 26, 243–247.[CrossRef][ISI][Medline]
Wilson, R.I., Turner, G.C. and Laurent, G. (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science, 303, 366–370.
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