全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Stimulus and Network Dynamics Collide in a Ratiometric Model of the Antennal Lobe Macroglomerular Complex

DOI: 10.1371/journal.pone.0029602

Full-Text   Cite this paper   Add to My Lib

Abstract:

Time is considered to be an important encoding dimension in olfaction, as neural populations generate odour-specific spatiotemporal responses to constant stimuli. However, during pheromone mediated anemotactic search insects must discriminate specific ratios of blend components from rapidly time varying input. The dynamics intrinsic to olfactory processing and those of naturalistic stimuli can therefore potentially collide, thereby confounding ratiometric information. In this paper we use a computational model of the macroglomerular complex of the insect antennal lobe to study the impact on ratiometric information of this potential collision between network and stimulus dynamics. We show that the model exhibits two different dynamical regimes depending upon the connectivity pattern between inhibitory interneurons (that we refer to as fixed point attractor and limit cycle attractor), which both generate ratio-specific trajectories in the projection neuron output population that are reminiscent of temporal patterning and periodic hyperpolarisation observed in olfactory antennal lobe neurons. We compare the performance of the two corresponding population codes for reporting ratiometric blend information to higher centres of the insect brain. Our key finding is that whilst the dynamically rich limit cycle attractor spatiotemporal code is faster and more efficient in transmitting blend information under certain conditions it is also more prone to interference between network and stimulus dynamics, thus degrading ratiometric information under naturalistic input conditions. Our results suggest that rich intrinsically generated network dynamics can provide a powerful means of encoding multidimensional stimuli with high accuracy and efficiency, but only when isolated from stimulus dynamics. This interference between temporal dynamics of the stimulus and temporal patterns of neural activity constitutes a real challenge that must be successfully solved by the nervous system when faced with naturalistic input.

References

[1]  Hansson BS (1999) pp. 125–161. Functional characteristics of the antennal lobe, Springer, chapter 5.
[2]  Murlis J, Elkinton JS, Carde RT (1992) Odor plumes and how insects use them. Annual Review of Entomology 37: 505–532.
[3]  Baker TC, Haynes KF (1996) Pheromone-mediated optomotor anemotaxis and altitude control exhibited by male oriental fruit moths in the field. Physiological Entomology 21: 20–32.
[4]  Hartlieb E, Anderson P (1999) pp. 315–349. Olfactory-released behaviours, Springer, chapter 11.
[5]  Valeur PG, Lofstedt C (1996) Behaviour of male oriental fruit moth, grapholita molesta, in overlapping sex pheromone plumes in a wind tunnel. Entomologia Experimentalis et Applicata 79: 51–59.
[6]  Kaissling K, Kramer E (1990) Sensory basis of pheromone-mediated orientation in moths. Verhandlungen der Deutschen Zoologischen Gesellschaft 83: 109–131.
[7]  Akers RP, O'Connell RJ (1988) The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male redbanded leafroller moths. Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology 163: 641–650.
[8]  Hansson BS, Ljungberg H, Hallberg E, Lofstedt C (1992) Functional specialization of olfactory glomeruli in a moth. Science 256: 1313–1315.
[9]  Carlsson MA, Galizia CG, Hansson BS (2002) Spatial representation of odours in the antennal lobe of the moth spodoptera littoralis (lepidoptera : Noctuidae). Chemical Senses 27: 231–244.
[10]  Wu WQ, Anton S, Lofstedt C, Hansson BS (1996) Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum. Proceedings of the National Academy of Sciences of the United States of America 93: 8022–8027.
[11]  Christensen TA, Mustaparta H, Hildebrand JG (1989) Discrimination of sex-pheromone blends in the olfactory system of the moth. Chemical Senses 14: 463–477.
[12]  Christensen TA, Hildebrand JG, Tumlinson JH, Doolittle RE (1989) Sex-pheromone blend of Manduca-sexta responses of central olfactory interneurons to antennal stimulation in male moths. Archives of Insect Biochemistry and Physiology 10: 281–291.
[13]  Hansson BS, Anton S (2000) Function and morphology of the antennal lobe: new developments. Annual Review of Entomology 45: 203–231.
[14]  Heinbockel T, Christensen TA, Hildebrand JG (2004) Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. Journal of Comparative Physiology A Neuroethology Sensory Neural and Behavioral Physiology 190: 1023–1037.
[15]  Chong KY (2007) Encoding of odour blends in the moth antennal lobe. PhD thesis, Department of Engineering, University of Leicester.
[16]  Rabinovich M, Huerta R, Volkovskii A, Abarbanel HDI, Stopfer M, et al. (2000) Dynamical coding of sensory information with competitive networks. Journal of Physiology-Paris 94: 465–471.
[17]  Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annual Review of Entomology 34: 477–501.
[18]  Akers RP, O'Connell RJ (1991) Response specificity of male olfactory receptor neurons for the major and minor components of a female pheromone blend. Physiological Entomology 16: 1–17.
[19]  Sun XJ, Tolbert LP, Hildebrand JG (1997) Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth manduca sexta: A laser scanning confocal and electron microscopic study. Journal of Comparative Neurology 379: 2–20.
[20]  Carlsson MA, Hansson BS (2002) Responses in highly selective sensory neurons to blends of pheromone components in the moth agrotis segetum. Journal of Insect Physiology 48: 443–451.
[21]  Kárpáti Z, Dekker T, Hansson B (2008) Reversed functional topology in the antennal lobe of the male european corn borer. The Journal of Experimental Biology 211: 2841–2848.
[22]  Mazor O, Laurent G (2005) Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48: 661–673.
[23]  Vickers NJ, Christensen TA, Baker TC, Hildebrand JG (2001) Odour-plume dynamics influence the brain's olfactory code. Nature 410: 466–470.
[24]  Balkovsky E, Shraiman BI (2002) Olfactory search at high reynolds number. Proceedings of the National Academy of Sciences of the United States of America 99: 12589–12593.
[25]  Capurro A, Baroni F, Olsson S, Kuebler L, Karout S, et al. (2011) Complex blend coding in the moth antennal lobe emerges from balanced random networks. Submitted.
[26]  Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbo G (2009) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601–612.
[27]  Root CM, Masuyama K, Green DS, Enell LE, Nassel DR, et al. (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59: 311–321.
[28]  Raman B, Joseph J, Tang J, Stopfer M (2010) Temporally diverse firing patterns in olfactory receptor neurons underlie spatiotemporal neural codes for odors. The Journal of Neuroscience 30: 1994–2006.
[29]  Av-Ron E (1994) Modeling olfactory neurons of the insect antennal lobe. Boston: Kluwer Academic Publishers. pp. 173–178.
[30]  Av-Ron E, Rospars JP (1995) Modeling insect olfactory neuron signaling by a network utilizing disinhibition. BioSystems 36: 101–108.
[31]  Av-Ron E, Vibert JF (1996) A model for temporal and intensity coding in insect olfaction by a network of inhibitory neurons. Biosystems 39: 241–250.
[32]  Linster C, Masson C, Kerszberg M, Personnaz L, Dreyfus G (1992) A formal model of the insect olfactory macroglomerulus: simulations and analytical results. In: Giles C, Hanson S, Cowan J, editors. pp. 239–252. Advances in neural information processing systems, 5. Morgan Kaufmann.
[33]  Linster C, Masson C, Kerszberg M, Personnaz L, Dreyfus G (1993) Computational diversity in a formal model of the insect olfactory macroglomerulus. Neural Computation 5: 228–241.
[34]  Linster C, Kerszberg M, C M (1994) pp. 179–184. Pheromone detection, ratio discrimination and oscillations: a new approach to olfactory coding., Kluwer Academic Publishers.
[35]  Linster C, Dreyfus G (1996) A model for pheromone discrimination in the insect antennal lobe: Investigation of the role of neuronal response pattern complexity. Chemical Senses 21: 19–27.
[36]  Zavada A, Buckley C, Martinez D, Rospars J, Nowotny T (2011) Competition-based model of pheromone component ratio detection in the moth. PLoS ONE 6: 1–12.
[37]  Huerta R, Rabinovich M (2004) Reproducible sequence generation in random neural ensembles. Phys Rev Lett 93: 1–4.
[38]  Muezzinoglu MK, Vergara A, Huerta R, Nowotny T, Rulkov N, et al. (2008) Artificial olfactory brain for mixture identification. NIPS 2008: 1121–1128.
[39]  Muezzinoglu M, Huerta R, Abarbanel H, Ryan M, Rabinovich M (2009) Chemosensor-driven artificial antennal lobe transient dynamics enable fast recognition and working memory. Neural Computation 21: 1018–1037.
[40]  Joerges J, Kuttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387: 285–288.
[41]  Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, et al. (2001) Odor encoding as an active, dynamical process: Experiments, computation, and theory. Annual Review of Neuroscience 24: 263–297.
[42]  Afraimovich VS, Rabinovich MI, Varona P (2004) Heteroclinic contours in neural ensembles and the winnerless competition principle. International Journal of Bifurcation and Chaos 14: 1195–1208.
[43]  Rabinovich M, Volkovskii A, Lecanda P, Huerta R, Abarbanel HDI, et al. (2001) Dynamical encoding by networks of competing neuron groups: Winnerless competition. Physical Review Letters 87: 068102.
[44]  Stopfer M, Jayaraman V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39: 991–1004.
[45]  Geffen M, Broome BM, Laurent G, Meister M (2009) Neural encoding of rapidly fluctuating odors. Neuron 61: 570–586.
[46]  Rabinovich M, Huerta R, Laurent G (2008) Transient dynamics for neural processing. Science 321: 48–50.
[47]  Niessing J, Friedrich RW (2010) Olfactory pattern classification by discrete neuronal network states. Nature 465: 47–52.
[48]  Heinbockel T, Christensen TA, Hildebrand JG (1999) Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth manduca sexta. Journal of Comparative Neurology 409: 1–12.
[49]  Brown SL, Joseph J, Stopfer M (2005) Encoding a temporally structured stimulus with a temporally structured neural representation. Nature Neuroscience 8: 1568–1576.
[50]  Galan RF, Sachse S, Galizia CG, Herz AVM (2004) Odor-driven attractor dynamics in the antennal lobe allow for simple and rapid olfactory pattern classification. Neural Computation 16: 999–1012.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133