Skip to main content
Log in

The "Where" and "Who" in Brain Science: Probing Brain Networks with Local Perturbations

  • Published:
Cognitive Computation Aims and scope Submit manuscript

Abstract

In a reductionistic approach to biology, the two important questions of "necessity" and "sufficiency" have been tremendously important for scientific progress. For example, to show the role of a particular gene, both knock-out mutants ("necessity") and rescue mutants ("sufficiency") need to be considered. These concepts, however, fail in combinatorial network situations. When emergent brain properties arise from the interaction of multiple brain areas, and redundant paths lead to resilience, then none of these areas can be identified as either "necessary" or "sufficient." Here, we use a relatively small-scale network—the glomerular odor-activity map—as a model for redundant combinatorial coding mechanisms. In particular, we use local interference with the functioning network with inhibitory and excitatory neuropharmacological injections to probe the resulting network perturbations. In vivo calcium imaging affords us with access to much of the network activity in real time. We observed, for example, that these local perturbations can generate physiological changes in distant places of the brain. This has important implications for our understanding of neural networks, in particular about the question of "where" a particular capacity—e.g., consciousness—is localized in the brain, and "who" (which cell) is involved. A related important question is "how" a function emerges, i.e., which neural networks are underlying this function? This issue can be addressed using combined functional and anatomical study of the network.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Shepherd G, Chen W, Greer C. Olfactory buld. In: Shepherd G, editor. The synaptic organization of the brain, chapter 5. Oxford: Oxford University Press; 2004. p. 165–216.

    Chapter  Google Scholar 

  2. Youngentob SL, Schwob JE, Sheehe PR, Youngentob LM. Odorant threshold following methyl bromide-induced lesions of the olfactory epithelium. Physiol Behav 1997;62:1241–52.

    Article  PubMed  CAS  Google Scholar 

  3. Hildebrand JG, Shepherd GM. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 1997;20:595–631.

    Article  PubMed  CAS  Google Scholar 

  4. Wilson RI, Mainen ZF. Early events in olfactory processing. Annu Rev Neurosci 2006;29:163–201.

    Article  PubMed  CAS  Google Scholar 

  5. Arnold G, Masson C, Budharugsa S. Comparative study of the antennal lobes and their in the worker bee and the drone (Apis mellifera). Cell Tissue Res 1985;242:593–605.

    Article  Google Scholar 

  6. Flanagan D, Mercer A. An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 1989;18:145–59.

    Article  Google Scholar 

  7. Galizia CG, McIlwrath SL, Menzel R. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 1999;295:383–94.

    Article  PubMed  CAS  Google Scholar 

  8. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 1999;405:543–52.

    Article  PubMed  CAS  Google Scholar 

  9. Couto A, Alenius M, Dickson BJ. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 2005;15:1535–47.

    Article  PubMed  CAS  Google Scholar 

  10. Fishilevich E, Vosshall LB. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 2005;15:1548–53.

    Article  PubMed  CAS  Google Scholar 

  11. Berg BG, Galizia CG, Brandt R, Mustaparta H. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 2002;446:123–34.

    Article  PubMed  Google Scholar 

  12. Greiner B, Gadenne C, Anton S. Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: a tool to study structure-function correlation. J Comp Neurol 2004;475:202–10.

    Article  PubMed  Google Scholar 

  13. Masante-Roca I, Gadenne C, Anton S. Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J Exp Biol 2005;208:1147–59.

    Article  PubMed  Google Scholar 

  14. Namiki S, Kanzaki R. Reconstructing the population activity of olfactory output neurons that innervate identifiable processing units. Front Neural Circuits 2008;2:1.

    Article  PubMed  Google Scholar 

  15. Ghaninia M, Hansson BS, Ignell R. The antennal lobe of the African malaria mosquito, Anopheles gambiae—innervation and three-dimensional reconstruction. Arthropod Struct Dev 2007;36:23–39.

    Article  PubMed  Google Scholar 

  16. Galizia CG, Sachse S, Rappert A, Menzel R. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 1999;2:473–8.

    Article  PubMed  CAS  Google Scholar 

  17. Sachse S, Rappert A, Galizia CG. The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 1999;11:3970–82.

    Article  PubMed  CAS  Google Scholar 

  18. Fernandez PC, Locatelli FF, Person-Rennell N, Deleo G, Smith BH. Associative conditioning tunes transient dynamics of early olfactory processing. J Neurosci 2009;29:10191–202.

    Article  PubMed  CAS  Google Scholar 

  19. Galizia LRCG, Szyszka P. Multiple memory traces after associative learning in the honey bee antennal lobe. Eur J Neurosci 2011;34:352–60.

    Article  Google Scholar 

  20. Hammer M. Multiple memory traces after associative learning in the honey bee antennal lobe. Nat Biotechnol 1993;366:59–63.

    Article  Google Scholar 

  21. Kreissl S, Eichmller S, Bicker G, Rapus J, Eckert M. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 1994;348:583–95.

    Article  PubMed  CAS  Google Scholar 

  22. Flanagan D, Mercer A. Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 1989;164:484–94.

    Article  Google Scholar 

  23. Mobbs P. Brain structure. In: Kerkut G, Gilbert L, editors. Comprehensive insect physiology biochemistry and pharmacology 5: nervous system: structure and motor function. Oxford: Pergamon Press; 1985. p. 299–370.

    Google Scholar 

  24. Rybak J, Menzel R. Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 1993;334:444–65.

    Article  PubMed  CAS  Google Scholar 

  25. Iwama A, Shibuya T. Physiology and morphology of olfactory neurons associating with the protocerebral lobe of the honeybee brain. J Insect Physiol 1998;44:1191–204.

    Article  PubMed  CAS  Google Scholar 

  26. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grnewald B, Rssler W. Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 2006;499:933–52.

    Article  PubMed  Google Scholar 

  27. Imai T, Sakano H, Vosshall LB. Topographic mapping—the olfactory system. Cold Spring Harb Perspect Biol 2010;2:a001776.

    Article  PubMed  Google Scholar 

  28. Fonta C, Sun X, Masson C. Morphology and spatial distribution of bee antennal lobe interneurones responsive to odors. Chem Senses 1993;18:101–19.

    Article  Google Scholar 

  29. Sun X, Fonta C, Masson C. Odour quality processing by bee antennal lobe neurons. Chem Senses 1993;18:355–77.

    Article  CAS  Google Scholar 

  30. Schäfer S, Bicker G. Distribution of gaba-like immunoreactivity in the brain of the honeybee. J Comp Neurol 1986;246:287–300.

    Google Scholar 

  31. Galizia CG, Menzel R. The role of glomeruli in the neural representation of odours: results from optical recording studies. J Insect Physiol 2001;47:115–30.

    Article  PubMed  CAS  Google Scholar 

  32. Galizia CG, Rössler W. Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 2010;55:399–420.

    Article  PubMed  CAS  Google Scholar 

  33. Root CM, Masuyama K, Green DS, Enell LE, Nssel DR, Lee CH, Wang JW. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 2008;59:311–21.

    Article  PubMed  CAS  Google Scholar 

  34. Sachse S, Galizia C. Topography and dynamics of the olfactory system. In: Grillner S, Graybiel A, editors. Microcircuits: the interface between neurons and global brain function, chapter 13. Cambridge: The MIT Press; 2006. p. 251–74.

    Google Scholar 

  35. Galán RF, Weidert M, Menzel R, Herz AVM, Galizia CG. Sensory memory for odors is encoded in spontaneous correlated activity between olfactory glomeruli. Neural Comput 2006;18:10–25.

    Article  PubMed  Google Scholar 

  36. Sachse S, Galizia CG. The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 2003;18:2119–32.

    Article  PubMed  Google Scholar 

  37. Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW. Propagation of olfactory information in Drosophila. Proc Natl Acad Sci USA 2007;104:11826–31.

    Article  PubMed  CAS  Google Scholar 

  38. Sachse S, Galizia CG. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 2002;87:1106–17.

    PubMed  Google Scholar 

  39. Silbering AF, Galizia CG. Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 2007;27:11966–77.

    Article  PubMed  CAS  Google Scholar 

  40. Olsen SR, Wilson RI. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 2008;452:956–60.

    Article  PubMed  CAS  Google Scholar 

  41. Linster C, Sachse S, Galizia CG. Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 2005;93:3410–7.

    Article  PubMed  Google Scholar 

  42. Lalley P. Microiontophoresis and pressure ejection. In: Windhorst U, Johansson H, editors. Modern techniques in neuroscience research. Berlin: Springer; 1999. p. 193–212.

    Chapter  Google Scholar 

  43. Erber J, Masuhr T, Menzel R. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol Entomol 1980;5:343–58.

    Article  Google Scholar 

  44. Hammer M, Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 1998;5:146–56.

    PubMed  CAS  Google Scholar 

  45. Devaud JM, Blunk A, Podufall J, Giurfa M, Grnewald B. Using local anaesthetics to block neuronal activity and map specific learning tasks to the mushroom bodies of an insect brain. Eur J Neurosci 2007;26:3193–206.

    Article  PubMed  Google Scholar 

  46. Hu A, Zhang W, Wang Z. Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc Natl Acad Sci USA 2010;107:10262–7.

    Article  PubMed  CAS  Google Scholar 

  47. Strowbridge BW. Role of cortical feedback in regulating inhibitory microcircuits. Ann N Y Acad Sci 2009;1170:270–4.

    Article  PubMed  CAS  Google Scholar 

  48. Grossman N, Poher V, Grubb MS, Kennedy GT, Nikolic K, McGovern B, Palmini RB, Gong Z, Drakakis EM, Neil MAA, Dawson MD, Burrone J, Degenaar P. Multi-site optical excitation using ChR2 and micro-LED array. J Neural Eng 2010;7:16004.

    Article  PubMed  Google Scholar 

  49. Dreosti E, Lagnado L. Optical reporters of synaptic activity in neural circuits. Exp Physiol 2011;96:4–12.

    Article  PubMed  Google Scholar 

  50. Grewe BF, Helmchen F. Optical probing of neuronal ensemble activity. Curr Opin Neurobiol 2009;19:520–9.

    Article  PubMed  CAS  Google Scholar 

  51. Keller A, Vosshall LB. Influence of odorant receptor repertoire on odor perception in humans and fruit flies. Proc Natl Acad Sci USA 2007;104:5614–9.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cyrille C. Girardin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Girardin, C.C., Galizia, C.G. The "Where" and "Who" in Brain Science: Probing Brain Networks with Local Perturbations. Cogn Comput 4, 63–70 (2012). https://doi.org/10.1007/s12559-011-9122-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12559-011-9122-3

Keywords

Navigation