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Strength in diversity: functional diversity among olfactory neurons of the same type

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Abstract

Most animals depend upon olfaction to find food, mates, and to avoid predators. An animal’s olfactory circuit helps it sense its olfactory environment and generate critical behavioral responses. The general architecture of the olfactory circuit, which is conserved across species, is made up of a few different neuronal types including first-order receptor neurons, second- and third-order neurons, and local interneurons. Each neuronal type differs in their morphology, physiology, and neurochemistry. However, several recent studies have suggested that there is intrinsic diversity even among neurons of the same type and that this diversity is important for neural function. In this review, we first examine instances of intrinsic diversity observed among individual types of olfactory neurons. Next, we review potential genetic and experience-based plasticity mechanisms that underlie this diversity. Finally, we consider the implications of intrinsic neuronal diversity for circuit function. Overall, we hope to highlight the importance of intrinsic diversity as a previously underestimated property of circuit function.

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References

  • Adesnik H, Br uns W, Taniguchi H, Huang ZJ, Scanziani M (2012) A neural circuit for spatial summation in visual cortex. Nature 490:226–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arneodo EM, Penikis KB, Rabinowitz N, Licata A, Cichy A, Zhang J, Bozza T, Rinberg D (2018) Stimulus dependent diversity and stereotypy in the output of an olfactory functional unit. Nat Commun 9:1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TTB, Dionne H, Abbott LF, Axel R, Tanimoto H, Rubin GM (2014) The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3

  • Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berck ME, Khandelwal A, Claus L, Hernandez-Nunez L, Si G, Tabone CJ, Li F, Truman JW, Fetter RD, Louis M, Samuel ADT, Cardona A (2016) The wiring diagram of a glomerular olfactory system. eLife 5

  • Bhalerao S, Sen A, Stocker R, Rodrigues V (2003) Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. J Neurobiol 54:577–592

    Article  PubMed  Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

    Article  CAS  PubMed  Google Scholar 

  • Boeckh J, Ernst KD, Selsam P (1987) Neurophysiology and neuroanatomy of the olfactory pathway in the cockroach. Ann N Y Acad Sci 510:39–43

    Article  CAS  PubMed  Google Scholar 

  • Bozza T, Feinstein P, Zheng C, Mombaerts P (2002) Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22:3033–3043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  CAS  PubMed  Google Scholar 

  • Carlson JR (1996) Olfaction in Drosophila: from odor to behavior. Trends Genet 12:175–180

    Article  CAS  PubMed  Google Scholar 

  • Chalasani SH, Chronis N, Tsunozaki M, Gray JM, Ramot D, Goodman MB, Bargmann CI (2007) Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450:63–70

    Article  CAS  PubMed  Google Scholar 

  • Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R (2011) Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1003–1014

    Article  CAS  Google Scholar 

  • Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Local interneurons and information-processing in the olfactory glomeruli of the moth Manduca-Sexta. J Comp Physiol A 173:385–399

    Article  CAS  PubMed  Google Scholar 

  • Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338

    Article  CAS  PubMed  Google Scholar 

  • Couto A, Alenius M, Dickson B (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol : CB 15:1535–1547

    Article  CAS  PubMed  Google Scholar 

  • Dalton RP, Lomvardas S (2015) Chemosensory receptor specificity and regulation. Annu Rev Neurosci 38(38):331–349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhawale AK, Hagiwara A, Bhalla US, Murthy VN, Albeanu DF (2010) Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci 13:1404–U1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endo K, Aoki T, Yoda Y, Kimura KI, Hama C (2007) Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 10:153–160

    Article  CAS  PubMed  Google Scholar 

  • Endo K, Karim MR, Taniguchi H, Krejci A, Kinameri E, Siebert M, Ito K, Bray SJ, Moore AW (2012) Chromatin modification of notch targets in olfactory receptor neuron diversification. Nat Neurosci 15:224–233

    Article  CAS  Google Scholar 

  • Fisek M, Wilson RI (2014) Stereotyped connectivity and computations in higher-order olfactory neurons. Nat Neurosci 17:280–288

    Article  CAS  PubMed  Google Scholar 

  • Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol : CB 15:1548–1553

    Article  CAS  PubMed  Google Scholar 

  • Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, Louis M (2005) Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol : CB 15:2086–2096

    Article  CAS  PubMed  Google Scholar 

  • Friedrich RW, Laurent G (2001) Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science 291:889–894

    Article  CAS  PubMed  Google Scholar 

  • Gerber B, Scherer S, Neuser K, Michels B, Hendel T, Stocker RF, Heisenberg M (2004) Visual learning in individually assayed Drosophila larvae. J Exp Biol 207:179–188

    Article  CAS  PubMed  Google Scholar 

  • Godfrey PA, Malnic B, Buck LB (2004) The mouse olfactory receptor gene family. Proc Natl Acad Sci U S A 101:2156–2161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golowasch J, Goldman MS, Abbott LF, Marder E (2002) Failure of averaging in the construction of a conductance-based neuron model. J Neurophysiol 87:1129–1131

    Article  PubMed  Google Scholar 

  • Gomez-Marin A, Louis M (2014) Multilevel control of run orientation in Drosophila larval chemotaxis. Front Behav Neurosci 8:38

  • Gomez-Marin A, Stephens GJ, Louis M (2011) Active sampling and decision making in Drosophila chemotaxis. Nat Commun 2:441

    Article  CAS  PubMed  Google Scholar 

  • Grabe V, Baschwitz A, Dweck HKM, Lavista-Llanos S, Hansson BS, Sachse S (2016) Elucidating the neuronal architecture of olfactory glomeruli in the Drosophila antennal lobe. Cell Rep 16:3401–3413

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Kunwar K, Smith D (2017) Odorant receptor sensitivity modulation in Drosophila. J Neurosci 37:9465–9473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160

    Article  CAS  PubMed  Google Scholar 

  • Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117:965–979

    Article  CAS  PubMed  Google Scholar 

  • Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF (2001) A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 98:15336–15341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Nunez L, Belina J, Klein M, Si G, Claus L, Carlson JR, Samuel AD (2015) Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics. eLife 4

  • Hige T, Aso Y, Rubin GM, Turner GC (2015) Plasticity-driven individualization of olfactory coding in mushroom body output neurons. Nature 526:258–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501

    Article  CAS  PubMed  Google Scholar 

  • Howell K, Hobert O (2017) Morphological diversity of C. elegans sensory cilia instructed by the differential expression of an immunoglobulin domain protein. Curr Biol 27:1782–1790.e5

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Zhang W, Qiao WH, Hu AQ, Wang ZR (2010) Functional connectivity and selective odor responses of excitatory local interneurons in Drosophila antennal lobe. Neuron 67:1021–1033

    Article  CAS  PubMed  Google Scholar 

  • Jones SV, Choi DC, Davis M, Ressler KJ (2008) Learning-dependent structural plasticity in the adult olfactory pathway. J Neurosci 28:13106–13111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaissling KE (2013) Kinetics of olfactory responses might largely depend on the odorant-receptor interaction and the odorant deactivation postulated for flux detectors. J Comp Physiol A 199:879–896

    Article  CAS  Google Scholar 

  • Kato A, Touhara K (2009) Mammalian olfactory receptors: pharmacology, G protein coupling and desensitization. Cell Mol Life Sci 66:3743–3753

    Article  CAS  PubMed  Google Scholar 

  • Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200

    Article  CAS  PubMed  Google Scholar 

  • Kay RB, Brunjes PC (2014) Diversity among principal and GABAergic neurons of the anterior olfactory nucleus. Front Cell Neurosci 8

  • Kenakin T (2017) Theoretical aspects of GPCR-ligand complex pharmacology. Chem Rev 117:4–20

    Article  CAS  PubMed  Google Scholar 

  • Kidd S, Lieber T (2016) Mechanism of notch pathway activation and its role in the regulation of olfactory plasticity in Drosophila melanogaster. PLoS One 11:e0151279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidd S, Struhl G, Lieber T (2015) Notch is required in adult Drosophila sensory neurons for morphological and functional plasticity of the olfactory circuit. PLoS Genet 11:e1005244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kikuta S, Fletcher ML, Homma R, Yamasoba T, Nagayama S (2013) Odorant response properties of individual neurons in an olfactory glomerular module. Neuron 77:1122–1135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim K, Kim JH, Song YH, Lee SH (2017) Functional dissection of inhibitory microcircuits in the visual cortex. Neurosci Res 116:70–76

    Article  CAS  PubMed  Google Scholar 

  • Kreher SA, Kwon JY, Carlson JR (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46:445–456

    Article  CAS  PubMed  Google Scholar 

  • Kreher SA, Mathew D, Kim J, Carlson JR (2008) Translation of sensory input into behavioral output via an olfactory system. Neuron 59:110–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larter NK, Sun JS, Carlson JR (2016) Organization and function of Drosophila odorant binding proteins. eLife 5

  • Laurent G (1996) Odor images and tunes. Neuron 16:473–476

    Article  CAS  PubMed  Google Scholar 

  • Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263–297

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES, Deisseroth K, Dan Y (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li QY, Ha TS, Okuwa S, Wang Y, Wang Q, Millard SS, Smith DP, Volkan PC (2013) Combinatorial rules of precursor specification underlying olfactory neuron diversity. Curr Biol 23:2481–2490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li QY, Barish S, Okuwa S, Maciejewski A, Brandt AT, Reinhold D, Jones CD, Volkan PC (2016) A functionally conserved gene regulatory network module governing olfactory neuron diversity. PLoS Genet 12:e1005780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtman JW, Sanes JR (2008) Ome sweet ome: what can the genome tell us about the connectome? Curr Opin Neurobiol 18:346–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieber T, Kidd S, Struhl G (2011) DSL-notch signaling in the Drosophila brain in response to olfactory stimulation. Neuron 69:468–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin D, Katz LC (2006) Representation of natural stimuli in the rodent main olfactory bulb. Chem Senses 31:A2–A2

    Google Scholar 

  • Liou NF et al (2018) Diverse populations of local interneurons integrate into the Drosophila adult olfactory circuit. Nat Commun 9

  • Liu AN, Urban NN (2017) Prenatal and early postnatal odorant exposure heightens odor-evoked mitral cell responses in the mouse olfactory bulb. Eneuro 4:ENEURO.0129–ENEU17.2017

    Google Scholar 

  • Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–366

    Article  CAS  PubMed  Google Scholar 

  • Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723

    Article  CAS  PubMed  Google Scholar 

  • Manzini I, Korsching S (2011) The peripheral olfactory system of vertebrates: molecular, structural and functional basics of the sense of smell. Neuroforum 17:110–118

    CAS  Google Scholar 

  • Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu CZ (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807

    Article  CAS  PubMed  Google Scholar 

  • Martelli C, Carlson JR, Emonet T (2013) Intensity invariant dynamics and odor-specific latencies in olfactory receptor neuron response. J Neurosci 33:6285–6297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masse NY, Turner GC, Jefferis GS (2009) Olfactory information processing in Drosophila. Curr Biol: CB 19:R700–R713

    Article  CAS  PubMed  Google Scholar 

  • Mathew D, Martelli C, Kelley-Swift E, Brusalis C, Gershow M, Samuel ADT, Emonet T, Carlson JR (2013) Functional diversity among sensory receptors in a Drosophila olfactory circuit. Proc Natl Acad Sci U S A 110:E2134–E2143

    Article  PubMed  PubMed Central  Google Scholar 

  • Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13:758–768

    Article  CAS  PubMed  Google Scholar 

  • Miles R (2000) Neurobiology - diversity in inhibition. Science 287:244–246

    Article  CAS  PubMed  Google Scholar 

  • Mo A, Mukamel EA, Davis FP, Luo C, Henry GL, Picard S, Urich MA, Nery JR, Sejnowski TJ, Lister R, Eddy SR, Ecker JR, Nathans J (2015) Epigenomic signatures of neuronal diversity in the mammalian brain. Neuron 86:1369–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mombaerts P (2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5:263–278

    Article  CAS  PubMed  Google Scholar 

  • Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686

    Article  CAS  PubMed  Google Scholar 

  • Montague SA, Mathew D, Carlson JR (2011) Similar odorants elicit different behavioral and physiological responses, some supersustained. J Neurosci 31:7891–7899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munch D, Galizia CG (2017) Take time: odor coding capacity across sensory neurons increases over time in Drosophila. J Comp Physiol A 203:959–972

    Article  Google Scholar 

  • Nagel KI, Wilson RI (2011) Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nat Neurosci 14:208–U296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagel KI, Wilson RI (2016) Mechanisms underlying population response dynamics in inhibitory interneurons of the Drosophila antennal lobe. J Neurosci 36:4325–4338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa T, Vosshall LB (2009) Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr Opin Neurobiol 19:284–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen SR, Bhandawat V, Wilson RI (2010) Divisive normalization in olfactory population codes. Neuron 66:287–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Padmanabhan K, Urban NN (2010) Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 13:1276–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parnas M, Lin AC, Huetteroth W, Miesenbock G (2013) Odor discrimination in Drosophila: from neural population codes to behavior. Neuron 79:932–944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prinz AA, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7:1345–1352

    Article  CAS  PubMed  Google Scholar 

  • Raja JSI, Katanayeva N, Katanaev VL, Galizia CG (2014) Role of G(o/i) subgroup of G proteins in olfactory signaling of Drosophila melanogaster. Eur J Neurosci 39:1245–1255

    Article  Google Scholar 

  • Ray A, van Naters WG, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray A, van Naters WV, Carlson JR (2008) A regulatory code for neuron-specific odor receptor expression. PLoS Biol 6:1069–1083

    Article  CAS  Google Scholar 

  • Ribich S, Tasic B, Maniatis T (2006) Identification of long-range regulatory elements in the protocadherin-alpha gene cluster. Proc Natl Acad Sci U S A 103:19719–19724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Root CM, Masuyama K, Green DS, Enell LE, Nassel DR, Lee CH, Wang JW (2008) A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Root CM, Denny CA, Hen R, Axel R (2014) The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515:269–U274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Vosshall LB (2007) Activity-dependent plasticity in an olfactory circuit. Neuron 56:838–850

    Article  CAS  PubMed  Google Scholar 

  • Saito H, Chi QY, Zhuang HY, Matsunami H, Mainland J (2009) Odor coding by a mammalian receptor repertoire. Neurosci Res 65:S76–S76

    Article  Google Scholar 

  • Sakano H (2010) Neural map formation in the mouse olfactory system. Neuron 67:530–542

    Article  CAS  PubMed  Google Scholar 

  • Santoro SW, Dulac C (2012) The activity-dependent histone variant H2BE modulates the life span of olfactory neurons. eLife 1

  • Sato K, Pellegrino M, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  CAS  PubMed  Google Scholar 

  • Schaefer AT, Larkum ME, Sakmann B, Roth A (2003) Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89:3143–3154

    Article  PubMed  Google Scholar 

  • Schneider D (1969) Insect olfaction: deciphering system for chemical messages. Science 163:1031–1037

    Article  CAS  PubMed  Google Scholar 

  • Schulz DJ, Goaillard JM, Marder E (2006) Variable channel expression in identified single and electrically coupled neurons in different animals. Nat Neurosci 9:356–362

    Article  CAS  PubMed  Google Scholar 

  • Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS (2010) Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104:1007–1019

    Article  PubMed  Google Scholar 

  • Seki Y, Dweck HKM, Rybak J, Wicher D, Sachse S, Hansson BS (2017) Olfactory coding from the periphery to higher brain centers in the Drosophila brain. BMC Biol 15:56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbock G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silbering AF, Benton R (2010) Ionotropic and metabotropic mechanisms in chemoreception: 'chance or design. EMBO Rep 11:173–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol Biol 38:770–780

    Article  CAS  PubMed  Google Scholar 

  • Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472:213–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanczyk NM, Brookfield JFY, Field LM, Logan JG (2013) Aedes aegypti mosquitoes exhibit decreased repellency by DEET following previous exposure. PLoS One 8:e54438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stiefel KM, Englitz B, Sejnowski TJ (2013) Origin of intrinsic irregular firing in cortical interneurons. Proc Natl Acad Sci U S A 110:7886–7891

    Article  PubMed  PubMed Central  Google Scholar 

  • Stocker R (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26

    Article  CAS  PubMed  Google Scholar 

  • Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34

    Article  CAS  PubMed  Google Scholar 

  • Su CY, Menuz K, Carlson JR (2009) Olfactory perception: receptors, cells, and circuits. Cell 139:45–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka NK, Awasaki T, Shimada T, Ito K (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol : CB 14:449–457

    Article  CAS  PubMed  Google Scholar 

  • Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755

    Article  PubMed  Google Scholar 

  • Taylor AL, Goaillard JM, Marder E (2009) How multiple Conductances determine electrophysiological properties in a multicompartment model. J Neurosci 29:5573–5586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, Garg K, John S, Sandstrom R, Bates D, Boatman L, Canfield TK, Diegel M, Dunn D, Ebersol AK, Frum T, Giste E, Johnson AK, Johnson EM, Kutyavin T, Lajoie B, Lee BK, Lee K, London D, Lotakis D, Neph S, Neri F, Nguyen ED, Qu H, Reynolds AP, Roach V, Safi A, Sanchez ME, Sanyal A, Shafer A, Simon JM, Song L, Vong S, Weaver M, Yan Y, Zhang Z, Zhang Z, Lenhard B, Tewari M, Dorschner MO, Hansen RS, Navas PA, Stamatoyannopoulos G, Iyer VR, Lieb JD, Sunyaev SR, Akey JM, Sabo PJ, Kaul R, Furey TS, Dekker J, Crawford GE, Stamatoyannopoulos JA (2012) The accessible chromatin landscape of the human genome. Nature 489:75–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobin WF, Wilson RI, Lee WCA (2017) Wiring variations that enable and constrain neural computation in a sensory microcircuit. eLife 6

  • Turner SL, Li N, Guda T, Githure J, Carde RT, Ray A (2011) Ultra-prolonged activation of CO2-sensing neurons disorients mosquitoes. Nature 474:87–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vetter P, Roth A, Hausser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926–937

    Article  CAS  PubMed  Google Scholar 

  • Vosshall LB (2000) Olfaction in Drosophila. Curr Opin Neurobiol 10:498–503

    Article  CAS  PubMed  Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    Article  CAS  PubMed  Google Scholar 

  • Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17:411–423

    Article  PubMed  Google Scholar 

  • Wang F, Nemes A, Mendelsohn M, Axel R (1998) Odorant receptors govern the formation of a precise topographic map. Cell 93:47–60

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    Article  CAS  PubMed  Google Scholar 

  • Wicher D, Schafer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452:1007–1011

    Article  CAS  PubMed  Google Scholar 

  • Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–370

    Article  CAS  PubMed  Google Scholar 

  • Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687–696

    Article  CAS  PubMed  Google Scholar 

  • Xia YF, Wang GR, Buscariollo D, Pitts RJ, Wenger H, Zwiebel LJ (2008) The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proc Natl Acad Sci U S A 105:6433–6438

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu PS, Lee D, Holy TE (2016) Experience-dependent plasticity drives individual differences in pheromone-sensing neurons. Neuron 91:878–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yagi T (2013) Genetic basis of neuronal individuality in the mammalian brain. J Neurogenet 27:97–105

    Article  PubMed  PubMed Central  Google Scholar 

  • Yao CA, Carlson JR (2010) Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila. J Neurosci 30:4562–4572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao HQ, Reed RR (2001) X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104:651–660

    Article  CAS  PubMed  Google Scholar 

  • Zufall F, Leinders-Zufall T (2000) The cellular and molecular basis of odor adaptation. Chem Senses 25:473–481

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are supported by a grant from the NIGMS of the National Institute of Health under grant number P20 GM103650 and by startup funds from the University of Nevada, Reno awarded to DM.

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Slankster, E., Odell, S.R. & Mathew, D. Strength in diversity: functional diversity among olfactory neurons of the same type. J Bioenerg Biomembr 51, 65–75 (2019). https://doi.org/10.1007/s10863-018-9779-3

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  • DOI: https://doi.org/10.1007/s10863-018-9779-3

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