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Organ der Neurowissenschaftlichen Gesellschaft

Editor-in-Chief: Wahle, Petra

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Volume 25, Issue 1


Neuromodulation of early sensory processing in the olfactory system

Neuromodulation der frühen sensorischen Verarbeitung im olfaktorischen System

Daniela Brunert
  • Corresponding author
  • Dept. Chemosensation – AG Neuromodulation RWTH Aachen University 52074 Aachen Aachen Germany
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  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Markus Rothermel
  • Corresponding author
  • Dept. Chemosensation – AG Neuromodulation RWTH Aachen University 52074 Aachen Aachen Germany
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2019-02-08 | DOI: https://doi.org/10.1515/nf-2018-0021


In jedem Moment sind wir von einer Vielzahl von Informationen umgeben, die gleichzeitig von mehreren Sinnen empfangen werden. Eine enorme Menge an Daten muss daher in unserem Gehirn gleichzeitig verarbeitet werden, um unsere Umwelt richtig zu verstehen. Eine Anpassung der sensorischen Verarbeitung ist wichtig, um unsere Wahrnehmung kontextabhängig optimieren zu können, d. h. um adäquate Verhaltensreaktionen zu ermöglichen, muss eine effiziente sensorische Verarbeitung relevanter Stimuli gefördert und unwichtige Signale unterdrückt werden. Die zugrundeliegenden Mechanismen der sensorischen Informationsmodulation sind, insbesondere in frühen sensorischen Schaltkreisen, weitgehend unbekannt. Die Fähigkeit, diese Prozesse selektiv manipulieren zu können, wäre sowohl für die Grundlagenforschung als auch die translationale biomedizinische Forschung von großem Vorteil. Hier betrachten wir das olfaktorische System der Vertebraten als Modellsystem für die Untersuchung früher sensorische Verarbeitung und demonstrieren die Komplexität neuromodulatorischer Vorgänge anhand dieses Systems.


At any given moment, we are continuously presented with information that is received from multiple sensory organs. Thus, our brain simultaneously processes enormous amounts of data in order to render an understanding of our environment. Adjustment of sensory processing is therefore important for tuning perception in a context-dependent fashion, i. e. to facilitate adequate behavioral responses by promoting the efficient sensory processing of relevant stimuli, while suppressing unimportant signals. The basic mechanisms that underlie the modulation of sensory information remain largely unknown, especially when considering early sensory circuits. Importantly, an ability to selectively manipulate these processes would offer great advantages for both basic and translational biomedical research. Here, we highlight the vertebrate olfactory bulb as a model system for early sensory processing and its utility in demonstrating the complexity of neuromodulatory actions.


  • Aqrabawi AJ, Kim JC (2018) Hippocampal projections to the anterior olfactory nucleus differentially convey spatiotemporal information during episodic odour memory. Nat Commun 9:2735.Google Scholar

  • Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629.Google Scholar

  • Babadi B, Sompolinsky H (2014) Sparseness and expansion in sensory representations. Neuron 83:1213–1226.Google Scholar

  • Balu R, Pressler RT, Strowbridge BW (2007) Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 27:5621–5632.Google Scholar

  • Banks WA, Kastin AJ, Pan W (1999) Uptake and degradation of blood-borne insulin by the olfactory bulb. Peptides 20:373–378.Google Scholar

  • Bendahmane M, Ogg MC, Ennis M, Fletcher ML (2016) Increased olfactory bulb acetylcholine bi-directionally modulates glomerular odor sensitivity. Sci Rep 6:25808.Google Scholar

  • Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174.Google Scholar

  • Boyd AM, Kato HK, Komiyama T, Isaacson JS (2015) Broadcasting of cortical activity to the olfactory bulb. Cell Rep 10:1032–1039.Google Scholar

  • Brunert D, Tsuno Y, Rothermel M, Shipley MT, Wachowiak M (2016) Cell-Type-Specific Modulation of Sensory Responses in Olfactory Bulb Circuits by Serotonergic Projections from the Raphe Nuclei. J Neurosci 36:6820–6835.Google Scholar

  • Bucher D, Marder E (2013) SnapShot: Neuromodulation. Cell 155:482–482 e481.Google Scholar

  • Carlsen J, Zaborszky L, Heimer L (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234:155–167.Google Scholar

  • Carson KA (1984) Quantitative localization of neurons projecting to the mouse main olfactory bulb. Brain Res Bull 12:629–634.Google Scholar

  • Case DT, Burton SD, Gedeon JY, Williams SG, Urban NN, Seal RP (2017) Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat Commun 8:652.Google Scholar

  • Chan W, Singh S, Keshav T, Dewan R, Eberly C, Maurer R, Nunez-Parra A, Araneda RC (2017) Mice Lacking M1 and M3 Muscarinic Acetylcholine Receptors Have Impaired Odor Discrimination and Learning. Front Synaptic Neurosci 9:4.Google Scholar

  • Chapuis J, Cohen Y, He X, Zhang Z, Jin S, Xu F, Wilson DA (2013) Lateral entorhinal modulation of piriform cortical activity and fine odor discrimination. J Neurosci 33:13449–13459.Google Scholar

  • Chaudhury D, Escanilla O, Linster C (2009) Bulbar acetylcholine enhances neural and perceptual odor discrimination. J Neurosci 29:52–60.Google Scholar

  • Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS (2013) Ultra-sensitive fluorescent proteins for imaging neuronal activity. Nature in press.Google Scholar

  • Cleland TA, Morse A, Yue EL, Linster C (2002) Behavioral models of odor similarity. Behav Neurosci 116:222–231.Google Scholar

  • D’Souza RD, Vijayaraghavan S (2014) Paying attention to smell: cholinergic signaling in the olfactory bulb. Front Synaptic Neurosci 6:21.Google Scholar

  • Davis BJ, Macrides F (1981) The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment, and piriform cortex to the main olfactory bulb in the hamster: an autoradiographic study. J Comp Neurol 203:475–493.Google Scholar

  • Davis BJ, Macrides F, Youngs WM, Schneider SP, Rosene DL (1978) Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Res Bull 3:59–72.Google Scholar

  • Devore S, Linster C (2012) Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front Behav Neurosci 6:52.Google Scholar

  • Doty RL, Bagla R, Kim N (1999) Physostigmine enhances performance on an odor mixture discrimination test. Physiol Behav 65:801–804.Google Scholar

  • Eckmeier D, Shea SD (2014) Noradrenergic plasticity of olfactory sensory neuron inputs to the main olfactory bulb. J Neurosci 34:15234–15243.Google Scholar

  • Esquivelzeta Rabell J, Mutlu K, Noutel J, Martin Del Olmo P, Haesler S (2017) Spontaneous Rapid Odor Source Localization Behavior Requires Interhemispheric Communication. Curr Biol 27:1542–1548 e1544.Google Scholar

  • Fadool DA, Tucker K, Phillips JJ, Simmen JA (2000) Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83:2332–2348.Google Scholar

  • Fast CD, McGann JP (2017) Amygdalar Gating of Early Sensory Processing through Interactions with Locus Coeruleus. J Neurosci 37:3085–3101.Google Scholar

  • Ferezou I, Bolea S, Petersen CC (2006) Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50:617–629.Google Scholar

  • Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP, Nicoll RA, Huang ZJ, Stryker MP (2014) A cortical circuit for gain control by behavioral state. Cell 156:1139–1152.Google Scholar

  • Genovese F, Bauersachs HG, Grasser I, Kupke J, Magin L, Daiber P, Nakajima J, Mohrlen F, Messlinger K, Frings S (2016) Possible role of calcitonin gene-related peptide in trigeminal modulation of glomerular microcircuits of the rodent olfactory bulb. Eur J Neurosci.PubMedGoogle Scholar

  • Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702.Google Scholar

  • Gore F, Schwartz EC, Brangers BC, Aladi S, Stujenske JM, Likhtik E, Russo MJ, Gordon JA, Salzman CD, Axel R (2015) Neural Representations of Unconditioned Stimuli in Basolateral Amygdala Mediate Innate and Learned Responses. Cell 162:134–145.Google Scholar

  • Gottfried JA (2010) Central mechanisms of odour object perception. Nat Rev Neurosci 11:628–641.Google Scholar

  • Grobman M, Dalal T, Lavian H, Shmuel R, Belelovsky K, Xu F, Korngreen A, Haddad R (2018) A Mirror-Symmetric Excitatory Link Coordinates Odor Maps across Olfactory Bulbs and Enables Odor Perceptual Unity. Neuron 99:800–813 e806.Google Scholar

  • Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576.Google Scholar

  • Haberly LB, Price JL (1977) The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res 129:152–157.Google Scholar

  • Halasz N, Shepherd GM (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10:579–619.Google Scholar

  • Hangya B, Ranade SP, Lorenc M, Kepecs A (2015) Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback. Cell 162:1155–1168.Google Scholar

  • Hardy A, Palouzier-Paulignan B, Duchamp A, Royet JP, Duchamp-Viret P (2005) 5-Hydroxytryptamine action in the rat olfactory bulb: in vitro electrophysiological patch-clamp recordings of juxtaglomerular and mitral cells. Neuroscience 131:717–731.Google Scholar

  • Henquin JC (2011) The dual control of insulin secretion by glucose involves triggering and amplifying pathways in beta-cells. Diabetes Res Clin Pract 93 Suppl 1:S27–31.Google Scholar

  • Hurley LM, Hall IC (2011) Context-dependent modulation of auditory processing by serotonin. Hear Res 279:74–84.Google Scholar

  • Igarashi KM, Ieki N, An M, Yamaguchi Y, Nagayama S, Kobayakawa K, Kobayakawa R, Tanifuji M, Sakano H, Chen WR, Mori K (2012) Parallel Mitral and Tufted Cell Pathways Route Distinct Odor Information to Different Targets in the Olfactory Cortex. The Journal of Neuroscience 32:7970–7985.Google Scholar

  • Irwin M, Greig A, Tvrdik P, Lucero MT (2015) PACAP modulation of calcium ion activity in developing granule cells of the neonatal mouse olfactory bulb. J Neurophysiol 113:1234–1248.Google Scholar

  • Jacob SN, Nienborg H (2018) Monoaminergic Neuromodulation of Sensory Processing. Front Neural Circuits 12:51.Google Scholar

  • Jing M et al. (2018) A genetically encoded fluorescent acetylcholine indicator for in vitro and in vivo studies. Nat Biotechnol 36:726–737.Google Scholar

  • Kalen P, Wiklund L (1989) Projections from the medial septum and diagonal band of Broca to the dorsal and central superior raphe nuclei: a non-cholinergic pathway. Exp Brain Res 75:401–416.Google Scholar

  • Kandel ER (2013) Principles of neural science, 5th Edition. New York: McGraw-Hill.Google Scholar

  • Kapoor V, Provost AC, Agarwal P, Murthy VN (2016) Activation of raphe nuclei triggers rapid and distinct effects on parallel olfactory bulb output channels. Nat Neurosci 19:271–282.Google Scholar

  • Kato HK, Chu MW, Isaacson JS, Komiyama T (2012) Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76:962–975.Google Scholar

  • Katz PS (1999) Beyond neurotransmission: neuromodulation and its importance for information processing. Osford; New York: Oxford University Press.Google Scholar

  • Kikuta S, Sato K, Kashiwadani H, Tsunoda K, Yamasoba T, Mori K (2010) Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. Proc Natl Acad Sci U S A 107:12363–12368.Google Scholar

  • Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660.Google Scholar

  • Kunze WA, Shafton AD, Kemm RE, McKenzie JS (1991) Effect of stimulating the nucleus of the horizontal limb of the diagonal band on single unit activity in the olfactory bulb. Neuroscience 40:21–27.Google Scholar

  • Kunze WA, Shafton AD, Kemm RE, McKenzie JS (1992) Olfactory bulb output neurons excited from a basal forebrain magnocellular nucleus. Brain Res 583:327–331.Google Scholar

  • Lecoq J, Tiret P, Najac M, Shepherd GM, Greer CA, Charpak S (2009) Odor-evoked oxygen consumption by action potential and synaptic transmission in the olfactory bulb. J Neurosci 29:1424–1433.Google Scholar

  • Lei H, Mooney R, Katz LC (2006) Synaptic Integration of Olfactory Information in Mouse Anterior Olfactory Nucleus. J Neurosci 26:12023–12032.Google Scholar

  • Leitner FC, Melzer S, Lutcke H, Pinna R, Seeburg PH, Helmchen F, Monyer H (2016) Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nat Neurosci 19:935–944.Google Scholar

  • Li G, Cleland TA (2013) A Two-Layer Biophysical Model of Cholinergic Neuromodulation in Olfactory Bulb. The Journal of Neuroscience 33:3037–3058.Google Scholar

  • Linster C, Escanilla O (2018) Noradrenergic effects on olfactory perception and learning. Brain Res.PubMedGoogle Scholar

  • Linster C, Wyble BP, Hasselmo ME (1999) Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. J Neurophysiol 81:2737–2742.Google Scholar

  • Liu Z, Zhou J, Li Y, Hu F, Lu Y, Ma M, Feng Q, Zhang JE, Wang D, Zeng J, Bao J, Kim JY, Chen ZF, El Mestikawy S, Luo M (2014) Dorsal raphe neurons signal reward through 5-HT and glutamate. Neuron 81:1360–1374.Google Scholar

  • Lizbinski KM, Dacks AM (2017) Intrinsic and Extrinsic Neuromodulation of Olfactory Processing. Front Cell Neurosci 11:424.Google Scholar

  • Lottem E, Lorincz ML, Mainen ZF (2016) Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex. J Neurosci 36:7–18.Google Scholar

  • Ma M, Luo M (2012) Optogenetic Activation of Basal Forebrain Cholinergic Neurons Modulates Neuronal Excitability and Sensory Responses in the Main Olfactory Bulb. J Neurosci 32:10105–10116.Google Scholar

  • Mandairon N, Ferretti CJ, Stack CM, Rubin DB, Cleland TA, Linster C (2006) Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. European Journal of Neuroscience 24:3234–3244.Google Scholar

  • Manella LC, Petersen N, Linster C (2017) Stimulation of the Locus Ceruleus Modulates Signal-to-Noise Ratio in the Olfactory Bulb. J Neurosci 37:11605–11615.Google Scholar

  • Maren S (2016) Parsing Reward and Aversion in the Amygdala. Neuron 90:209–211.Google Scholar

  • Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76:1175–1188.Google Scholar

  • Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, Gordus A, Renninger SL, Chen T-W, Bargmann CI, Orger MB, Schreiter ER, Demb JB, Gan W-B, Hires SA, Looger LL (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Meth 10:162–170.Google Scholar

  • Marvin JS et al. (2018) Stability, affinity, and chromatic variants of the glutamate sensor iGluSnFR. Nat Methods.PubMedGoogle Scholar

  • Matsutani S, Yamamoto N (2008) Centrifugal innervation of the mammalian olfactory bulb. Anat Sci Int 83:218–227.Google Scholar

  • McClard CK, Arenkiel BR (2018) Neuropeptide Signaling Networks and Brain Circuit Plasticity. J Exp Neurosci 12:1179069518779207.Google Scholar

  • McGann JP (2017) Poor human olfaction is a 19th-century myth. Science 356.Google Scholar

  • McLachlan N, Wilson S (2010) The central role of recognition in auditory perception: a neurobiological model. Psychol Rev 117:175–196.Google Scholar

  • McLean JH, Shipley MT (1987) Serotonergic afferents to the rat olfactory bulb: I. Origins and laminar specificity of serotonergic inputs in the adult rat. J Neurosci 7:3016–3028.Google Scholar

  • McLean JH, Shipley MT, Nickell WT, Aston-Jones G, Reyher CK (1989) Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J Comp Neurol 285:339–349.Google Scholar

  • Miller JE, Granados-Fuentes D, Wang T, Marpegan L, Holy TE, Herzog ED (2014) Vasoactive intestinal polypeptide mediates circadian rhythms in mammalian olfactory bulb and olfaction. J Neurosci 34:6040–6046.Google Scholar

  • Miranda-Martinez A, Mercado-Gomez OF, Arriaga-Avila V, Guevara-Guzman R (2017) Distribution of Adiponectin Receptors 1 and 2 in the Rat Olfactory Bulb and the Effect of Adiponectin Injection on Insulin Receptor Expression. Int J Endocrinol 2017:4892609.Google Scholar

  • Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9:951–963.Google Scholar

  • Oettl LL, Ravi N, Schneider M, Scheller MF, Schneider P, Mitre M, da Silva Gouveia M, Froemke RC, Chao MV, Young WS, Meyer-Lindenberg A, Grinevich V, Shusterman R, Kelsch W (2016) Oxytocin Enhances Social Recognition by Modulating Cortical Control of Early Olfactory Processing. Neuron 90:609–621.Google Scholar

  • Otazu GH, Chae H, Davis MB, Albeanu DF (2015) Cortical Feedback Decorrelates Olfactory Bulb Output in Awake Mice. Neuron 86:1461–1477.Google Scholar

  • Palouzier-Paulignan B, Lacroix MC, Aime P, Baly C, Caillol M, Congar P, Julliard AK, Tucker K, Fadool DA (2012) Olfaction under metabolic influences. Chem Senses 37:769–797.Google Scholar

  • Parikh V, Sarter M (2008) Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity. Ann N Y Acad Sci 1129:225–235.Google Scholar

  • Patriarchi T, Cho JR, Merten K, Howe MW, Marley A, Xiong WH, Folk RW, Broussard GJ, Liang R, Jang MJ, Zhong H, Dombeck D, von Zastrow M, Nimmerjahn A, Gradinaru V, Williams JT, Tian L (2018) Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors. Science 360.Google Scholar

  • Pinching AJ, Powell TPS (1972) Termination of Centrifugal Fibers in Glomerular Layer of Olfactory Bulb. Journal of Cell Science 10:621-&.Google Scholar

  • Pressler RT, Strowbridge BW (2006) Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49:889–904.Google Scholar

  • Price JL, Powell TP (1970) An experimental study of the origin and the course of the centrifugal fibres to the olfactory bulb in the rat. J Anat 107:215–237.Google Scholar

  • Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259.Google Scholar

  • Retson TA, Van Bockstaele EJ (2013) Coordinate regulation of noradrenergic and serotonergic brain regions by amygdalar neurons. J Chem Neuroanat 52:9–19.Google Scholar

  • Reynolds JH, Chelazzi L (2004) Attentional modulation of visual processing. Annu Rev Neurosci 27:611–647.Google Scholar

  • Root CM, Denny CA, Hen R, Axel R (2014) The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515:269–273.Google Scholar

  • Rothermel M, Wachowiak M (2014) Functional imaging of cortical feedback projections to the olfactory bulb. Front Neural Circuits 8:73.Google Scholar

  • Rothermel M, Carey RM, Puche A, Shipley MT, Wachowiak M (2014) Cholinergic inputs from Basal forebrain add an excitatory bias to odor coding in the olfactory bulb. J Neurosci 34:4654–4664.Google Scholar

  • Salomon RM, Cowan RL (2013) Oscillatory serotonin function in depression. Synapse 67:801–820.Google Scholar

  • Sarafoleanu C, Mella C, Georgescu M, Perederco C (2009) The importance of the olfactory sense in the human behavior and evolution. J Med Life 2:196–198.Google Scholar

  • Schneider SP, Scott JW (1983) Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. J Neurophysiol 50:358–378.Google Scholar

  • Schoenfeld TA, Macrides F (1984) Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster. J Comp Neurol 227:121–135.Google Scholar

  • Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12:669–688.Google Scholar

  • Soria-Gomez E et al. (2014) The endocannabinoid system controls food intake via olfactory processes. Nat Neurosci 17:407–415.Google Scholar

  • Soudry Y, Lemogne C, Malinvaud D, Consoli SM, Bonfils P (2011) Olfactory system and emotion: common substrates. Eur Ann Otorhinolaryngol Head Neck Dis 128:18–23.Google Scholar

  • Spangler SM, Bruchas MR (2017) Optogenetic approaches for dissecting neuromodulation and GPCR signaling in neural circuits. Curr Opin Pharmacol 32:56–70.Google Scholar

  • Spors H, Albeanu DF, Murthy VN, Rinberg D, Uchida N, Wachowiak M, Friedrich RW (2012) Illuminating Vertebrate Olfactory Processing. J Neurosci 32:14102–14108.Google Scholar

  • Srinivasan S, Greenspan RJ, Stevens CF, Grover D (2018) Deep(er) Learning. J Neurosci 38:7365–7374.Google Scholar

  • Staubli U, Ivy G, Lynch G (1984) Hippocampal denervation causes rapid forgetting of olfactory information in rats. Proc Natl Acad Sci U S A 81:5885–5887.Google Scholar

  • Steinfeld R, Herb JT, Sprengel R, Schaefer AT, Fukunaga I (2015) Divergent innervation of the olfactory bulb by distinct raphe nuclei. J Comp Neurol 523:805–813.Google Scholar

  • Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347–370.Google Scholar

  • Strowbridge BW (2009) Role of cortical feedback in regulating inhibitory microcircuits. Ann N Y Acad Sci 1170:270–274.Google Scholar

  • Thornhill R, Gangestad SW, Miller R, Scheyd G, McCollough JK, Franklin M (2003) Major histocompatibility complex genes, symmetry, and body scent attractiveness in men and women. Behavioral Ecology 14:668–678.Google Scholar

  • Ueno M, Dobrogowska DH, Vorbrodt AW (1996) Immunocytochemical evaluation of the blood-brain barrier to endogenous albumin in the olfactory bulb and pons of senescence-accelerated mice (SAM). Histochem Cell Biol 105:203–212.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.Google Scholar

  • Wachowiak M, Economo MN, Díaz-Quesada M, Brunert D, Wesson DW, White JA, Rothermel M (2013) Optical Dissection of Odor Information Processing In Vivo Using GCaMPs Expressed in Specified Cell Types of the Olfactory Bulb. J Neurosci 33:5285–5300.Google Scholar

  • Wacker DW, Engelmann M, Tobin VA, Meddle SL, Ludwig M (2011) Vasopressin and social odor processing in the olfactory bulb and anterior olfactory nucleus. Ann N Y Acad Sci 1220: 106–116.Google Scholar

  • Waterhouse BD, Navarra RL (2018) The locus coeruleus-norepinephrine system and sensory signal processing: A historical review and current perspectives. Brain Res.PubMedGoogle Scholar

  • Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519.Google Scholar

  • Woolf NJ, Eckenstein F, Butcher LL (1984) Cholinergic systems in the rat brain: I. projections to the limbic telencephalon. Brain Res Bull 13:751–784.Google Scholar

  • Yu GZ, Kaba H, Okutani F, Takahashi S, Higuchi T (1996) The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 72:1083–1088.Google Scholar

  • Zald DH, Pardo JV (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci U S A 94:4119–4124.Google Scholar

  • Zelano C, Sobel N (2005) Humans as an animal model for systems-level organization of olfaction. Neuron 48: 431–454.Google Scholar

  • Zhan X, Yin P-b, Heinbockel T (2013) The Basal Forebrain Modulates Spontaneous Activity of Principal Cells in the Main Olfactory Bulb of Anaesthetized Mice. Frontiers in Neural Circuits 7.Google Scholar

  • Zimmer LA, Ennis M, Shipley MT (1999) Diagonal band stimulation increases piriform cortex neuronal excitability in vivo. Neuroreport 10:2101–2105.Google Scholar

About the article

Daniela Brunert

Daniela Brunert studied biology at the Ruhr University in Bochum and received her Ph.D. from the International Graduate School at the RUB working on neuromodulation in the mouse olfactory epithelium. She received postdoctoral training at the University of Florida under the supervision of Barry Ache, where she received a Feodor Lynen Fellowship and the University of Utah under the supervision of Matt Wachowiak where she was awarded the Young Investigator Award of the Association for Chemoreception Sciences for her work on serotonergic modulation of the olfactory bulb. After working briefly in the lab of Thomas Pap at the WWU Münster she joined the lab of Markus Rothermel at the RWTH Aachen.

Markus Rothermel

Markus Rothermel studied biology at the Ruhr University Bochum. His doctoral thesis with Hanns Hatt at the Department of Cellphysiology focused on “trigeminal perception” and was funded by scholarships from the research training group GRK 736, the Wilhelm and Günther Esser-Foundation and the Ruhr-University Research School. For his postdoctoral time he joined the laboratory of Matt Wachowiak (Boston University and the University of Utah, USA) focusing on information processing in the rodent olfactory system, a project for which he was awarded a DFG research fellowship. In October 2014, he returned to Germany in order to establish an Emmy Noether research group funded by the German Research Foundation at the RWTH Aachen University. His main interests are a systematic investigation of sensory filtering processes in health and disease.

Published Online: 2019-02-08

Published in Print: 2019-02-07

Citation Information: Neuroforum, Volume 25, Issue 1, Pages 25–37, ISSN (Online) 2363-7013, ISSN (Print) 0947-0875, DOI: https://doi.org/10.1515/nf-2018-0021.

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