Skip to main content
Log in

Olfactory-induced locomotion in lampreys

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The olfactory system allows animals to navigate in their environment to feed, mate, and escape predators. It is well established that odorant exposure or electrical stimulation of the olfactory system induces stereotyped motor responses in fishes. However, the neural circuitry responsible for the olfactomotor transformations is only beginning to be unraveled. A neural substrate eliciting motor responses to olfactory inputs was identified in the lamprey, a basal vertebrate used extensively to examine the neural mechanisms underlying sensorimotor transformations. Two pathways were discovered from the olfactory organ in the periphery to the brainstem motor nuclei responsible for controlling swimming. The first pathway originates from sensory neurons located in the accessory olfactory organ and reaches a single population of projection neurons in the medial olfactory bulb, which, in turn, transmit the olfactory signals to the posterior tuberculum and then to downstream brainstem locomotor centers. A second pathway originates from the main olfactory epithelium and reaches the main olfactory bulb, the neurons of which project to the pallium/cortex. The olfactory signals are then conveyed to the posterior tuberculum and then to brainstem locomotor centers. Olfactomotor behavior can adapt, and studies were aimed at defining the underlying neural mechanisms. Modulation of bulbar neural activity by GABAergic, dopaminergic, and serotoninergic inputs is likely to provide strong control over the hardwired circuits to produce appropriate motor behavior in response to olfactory cues. This review summarizes current knowledge relative to the neural circuitry producing olfactomotor behavior in lampreys and their modulatory mechanisms.

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
Fig. 3

Similar content being viewed by others

References

  • Abalo XM, Villar-Cheda B, Anadón R, Rodicio MC (2005) Development of the dopamine-immunoreactive system in the central nervous system of the sea lamprey. Brain Res Bull 66:560–564

    Article  CAS  PubMed  Google Scholar 

  • Abalo XM, Villar-Cheda B, Meléndez-Ferro M, Pérez-Costas E, Anadón R, Rodicio MC (2007) Development of the serotonergic system in the central nervous system of the sea lamprey. J Chem Neuroanat 34:29–46

    Article  CAS  PubMed  Google Scholar 

  • Andersson O, Forssberg H, Grillner S, Lindquist M (1978) Phasic gain control of the transmission in cutaneous reflex pathways to motoneurones during fictive locomotion. Brain Res 149:503–507

    Article  CAS  PubMed  Google Scholar 

  • Antri M, Cyr A, Auclair F, Dubuc R (2006) Ontogeny of 5-HT neurons in the brainstem of the lamprey, Petromyzon marinus. J Comp Neurol 495:788–800

    Article  PubMed  Google Scholar 

  • Baumgarten HG (1972) Biogenic monoamines in the cyclostome and lower vertebrate brain. Prog Histochem Cytochem 4:1–90

    Article  CAS  PubMed  Google Scholar 

  • Beauséjour PA, Auclair F, Daghfous G, Ngovandan C, Veilleux D, Zielinski BS, Dubuc R (2020) Dopaminergic modulation of olfactory-evoked motor output in sea lampreys (Petromyzon marinus L.). J Comp Neurol 528:114–134

    Article  PubMed  Google Scholar 

  • Belluscio L, Gold GH, Nemes A, Axel R (1998) Mice deficient in G(olf) are anosmic. Neuron 20:69–81

    Article  CAS  PubMed  Google Scholar 

  • Bjerselius R, Li W, Teeter JH, Seelye JG, Johnsen PB, Maniak PJ, Grant GC, Polkinghorne CN, Sorensen PW (2000) Direct behavioral evidence that unique bile acids released by larval sea lamprey (Petromyzon marinus) function as a migratory pheromone. Can J Fish Aquat Sci 57:557–569

    Article  CAS  Google Scholar 

  • Blundell JE (1977) Is there a role for serotonin (5-hydroxytryptamine) in feeding? Int J Obes 1:15–42

    CAS  PubMed  Google Scholar 

  • Bouvier J, Caggiano V, Leiras R, Caldeira V, Bellardita C, Balueva K, Fuchs A, Kiehn O (2015) Descending command neurons in the brainstem that halt locomotion. Cell 163:1191–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyes K (2014) Serotonergic modulation of odour-evoked neural activity in the olfactory bulb of the sea lamprey (Petromyzon marinus). MSc thesis, Biological Sciences, University of Windsor

  • Breer H, Fleischer J, Strotmann J (2006) The sense of smell: multiple olfactory subsystems. Cell Mol Life Sci 63:1465–1475

    Article  CAS  PubMed  Google Scholar 

  • Brocard F, Dubuc R (2003) Differential contribution of reticulospinal cells to the control of locomotion induced by the mesencephalic locomotor region. J Neurophysiol 90:1714–1727

    Article  PubMed  Google Scholar 

  • Brocard F, Ryczko D, Fénelon K, Hatem R, Gonzales D, Auclair F, Dubuc R (2010) The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J Neurosci 30:523–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan JT, Grillner S (1987) Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord. Science 236:312–314

    Article  CAS  PubMed  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 

  • Capelli P, Pivetta C, Espósito MS, Arber S (2017) Locomotor speed control circuits in the caudal brainstem. Nature 551:373–377

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Chung-Davidson YW, Libants SV, Nanlohy KG, Kiupel M, Brown CT, Li W (2013) The sea lamprey has a primordial accessory olfactory system. BMC Evol Biol 13:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornide-Petronio ME, Anadón R, Barreiro-Iglesias A, Rodicio MC (2013) Serotonin 1A receptor (5-HT1A) of the sea lamprey: cDNA cloning and expression in the central nervous system. Brain Struct Funct 218:1317–1335

    Article  CAS  PubMed  Google Scholar 

  • Daghfous G, Auclair F, Clotten F, Létourneau JL, Atallah E, Millette JP, Derjean D, Robitaille R, Zielinski BS, Dubuc R (2018) GABAergic modulation of olfactomotor transmission in lampreys. PLoS Biol 16:e2005512

  • Derjean D, Moussaddy A, Atallah E, St-Pierre M, Auclair F, Chang S, Ren X, Zielinski BS, Dubuc R (2010) A novel neural substrate for the transformation of olfactory inputs into motor output. PLoS Biol 8:e1000567

  • Di Rocco RT, Belanger CF, Imre I, Brown GE, Johnson NS (2014) Daytime avoidance of chemosensory alarm cues by adult sea lamprey (Petromyzon marinus). Can J Fish Aquat Sci 71:824–830

    Article  Google Scholar 

  • Dubuc R, Brocard F, Antri M, Fénelon K, Gariépy JF, Smetana R, Ménard A, Le Ray D, Viana Di Prisco G, Pearlstein E, Sirota MG, Derjean D, St-Pierre M, Zielinski BS, Auclair F, Veilleux D (2008) Initiation of locomotion in lampreys. Brain Res Rev 57:172–182

    Article  PubMed  Google Scholar 

  • El Manira A, Pombal MA, Grillner S (1997) Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389:603–616

    Article  PubMed  Google Scholar 

  • Ericsson J, Stephenson-Jones M, Pérez-Fernández J, Robertson B, Silberberg G, Grillner S (2013) Dopamine differentially modulates the excitability of striatal neurons of the direct and indirect pathways in lamprey. J Neurosci 33:8045–8054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falck B (1962) Observation on the possibility of cellular localization of monoamines by a fluorescence method. Acta Physiol Scand 56:1–26

    Google Scholar 

  • Fletcher PJ (1988) Increased food intake in satiated rats induced by the 5-HT antagonists methysergide, metergoline and ritanserin. Psychopharmacology 96:237–242

    Article  CAS  PubMed  Google Scholar 

  • Freitag J, Beck A, Ludwig G, von Buchholtz L, Breer H (1999) On the origin of the olfactory receptor family: receptor genes of the jawless fish (Lampetra fluviatilis). Gene 226:165–174

    Article  CAS  PubMed  Google Scholar 

  • Frontini A, Zaidi AU, Hua H, Wolak TP, Greer CA, Kafitz KW, Li W, Zielinski BS (2003) Glomerular territories in the olfactory bulb from the larval stage of the sea lamprey Petromyzon marinus. J Comp Neurol 465:27–37

    Article  PubMed  Google Scholar 

  • Galizia CG, Rossler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    Article  CAS  PubMed  Google Scholar 

  • Grätsch S, Büschges A, Dubuc R (2019) Descending control of locomotor circuits. Current Opinion in Physiology 8:94–98

    Article  Google Scholar 

  • Grätsch S, Auclair F, Demers O, Auguste E, Hanna A, Büschges A, Dubuc R (2019) A brainstem neural substrate for stopping locomotion. J Neurosci 39:1044–1057

    Article  PubMed  PubMed Central  Google Scholar 

  • Green WW, Basilious A, Dubuc R, Zielinski BS (2013) The neuroanatomical organization of projection neurons associated with different olfactory bulb pathways in the sea lamprey, Petromyzon marinus. PLoS One 8:e69525

  • Green WW, Boyes K, McFadden C, Daghfous G, Auclair F, Zhang H, Li W, Dubuc R, Zielinski BS (2017) Odorant organization in the olfactory bulb of the sea lamprey. J Exp Biol 220:1350–1359

    PubMed  Google Scholar 

  • Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brooks VB (ed) Handbook of physiology, sect. 1. The nervous system II. Motor control. American Physiological Society, Waverly Press, pp 1179–1236

  • Grillner S, Kozlov A, Dario P, Stefanini C, Menciassi A, Lansner A, Hellgren Kotaleski J (2007) Modeling a vertebrate motor system: pattern generation, steering and control of body orientation. Prog Brain Res 165:221–234

    Article  PubMed  Google Scholar 

  • Grillner S, Robertson B, Stephenson-Jones M (2013) The evolutionary origin of the vertebrate basal ganglia and its role in action selection. J Physiol 591:5425–5431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grillner S, Robertson B (2016) The basal ganglia over 500 million years. Curr Biol 26:R1088–R1100

    Article  CAS  PubMed  Google Scholar 

  • Grillner S, El Manira A (2020) Current principles of motor control, with special reference to vertebrate locomotion. Physiol Rev 100:271–320

    Article  PubMed  Google Scholar 

  • Grimm RJ (1960) Feeding behavior and electrical stimulation of the brain of Carassius auratus. Science 131:162–163

    Article  CAS  PubMed  Google Scholar 

  • Grus WE, Zhang J (2009) Origin of the genetic components of the vomeronasal system in the common ancestor of all extant vertebrates. Mol Biol Evol 26:407–419

    Article  CAS  PubMed  Google Scholar 

  • Hagelin LO, Johnels AG (1955) On the structure and function of the accessory olfactory organ in lampreys. Acta Zool 36:113–125

    Article  Google Scholar 

  • Hansen A, Rolen SH, Anderson K, Morita Y, Caprio J, Finger TE (2003) Correlation between olfactory receptor cell type and function in the channel catfish. J Neurosci 23:9328–9339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashiguchi Y, Nishida M (2007) Evolution of trace amine associated receptor (TAAR) gene family in vertebrates: lineage-specific expansions and degradations of a second class of vertebrate chemosensory receptors expressed in the olfactory epithelium. Mol Biol Evol 24:2099–2107

    Article  CAS  PubMed  Google Scholar 

  • Heier P (1948) Fundamental principles in the structure of the brain. A study of the brain of Petromyzon fluviatilis. Acta Anat (Basel) 8:3–213

    Google Scholar 

  • Hoyer D, Clarke DE, Fozard JR, Hartig PR, Martin GR, Mylecharane EJ, Saxena PR, Humphrey PP (1994) International union of pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol Rev 46:157–203

    CAS  PubMed  Google Scholar 

  • Jacobson L (1811) Description anatomique d’un organe observé dans les mammifères. Ann Mus Hist Nat Paris 18:2–424

    Google Scholar 

  • Johnson NS, Luehring MA, Siefkes MJ, Li W (2006) Mating pheromone reception and induced behavior in ovulating female sea lampreys. N Am J Fish Manag 26:88–96

    Article  Google Scholar 

  • Johnson NS, Yun SS, Thompson HT, Brant CO, Li W (2009) A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps. Proc Natl Acad Sci 106:1021–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson NS, Yun SS, Buchinger TJ, Li W (2012) Multiple functions of a multi-component mating pheromone in sea lamprey Petromyzon marinus. J Fish Biol 80:538–554

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Reed RR (1989) Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science 244:790–795

    Article  CAS  PubMed  Google Scholar 

  • Juvin L, Grätsch S, Trillaud-Doppia E, Gariépy JF, Büschges A, Dubuc R (2016) A specific population of reticulospinal neurons controls the termination of locomotion. Cell Rep 15:2377–2386

    Article  CAS  PubMed  Google Scholar 

  • Kleerekoper H, Mogensen J (1963) Role of olfaction in the orientation of Petromyzon marinus. I. Response to a single amine in prey’s body odor. Physiol Zool 36:347–360

    Article  Google Scholar 

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920

    Article  CAS  PubMed  Google Scholar 

  • Laframboise AJ, Ren X, Chang S, Dubuc R, Zielinski BS (2007) Olfactory sensory neurons in the sea lamprey display polymorphisms. Neurosci Lett 414:277–281

    Article  CAS  PubMed  Google Scholar 

  • Le Ray D, Brocard F, Bourcier-Lucas C, Auclair F, Lafaille P, Dubuc R (2003) Nicotinic activation of reticulospinal cells involved in the control of swimming in lampreys. Eur J Neurosci 17:137–148

    Article  PubMed  Google Scholar 

  • Le Ray D, Juvin L, Ryczko D, Dubuc R (2011) Chapter 4--supraspinal control of locomotion: the mesencephalic locomotor region. Prog Brain Res 188:51–70

  • Li W (1994) Olfactory biology of adult sea lamprey (Petromyzon marinus). PhD thesis, University of Minnesota

  • Li W, Sorensen PW, Gallaher DD (1995) The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae. J Gen Physiol 105:569–587

    Article  CAS  PubMed  Google Scholar 

  • Li W, Sorensen PW (1997) Highly independent olfactory receptor sites for naturally occurring bile acids in the sea lamprey, Petromyzon marinus. J Comp Physiol A 180:429–438

    Article  CAS  Google Scholar 

  • Libants S, Carr K, Wu H, Teeter JH, Chung-Davidson YW, Zhang Z, Wilkerson C, Li W (2009) The sea lamprey Petromyzon marinus genome reveals the early origin of several chemosensory receptor families in the vertebrate lineage. BMC Evol Biol 9:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Marciello M, Sinnamon HM (1990) Locomotor stepping initiated by glutamate injections into the hypothalamus of the anesthetized rat. Behav Neurosci 104:980–990

    Article  CAS  PubMed  Google Scholar 

  • Matz SP (1995) Connections of the olfactory bulb in the chinook salmon (Oncorhynchus tshawytscha). Brain Behav Evol 46:108–120

    Article  CAS  PubMed  Google Scholar 

  • Meléndez-Ferro M, Pérez-Costas E, Rodríguez-Muñoz R, Gómez-López MP, Anadón R, Rodicio MC (2001) GABA immunoreactivity in the olfactory bulbs of the adult sea lamprey Petromyzon marinus L. Brain Res 893:253–260

    Article  PubMed  Google Scholar 

  • Ménard A, Auclair F, Bourcier-Lucas C, Grillner S, Dubuc R (2007) Descending GABAergic projections to the mesencephalic locomotor region in the lamprey Petromyzon marinus. J Comp Neurol 501:260–273

    Article  PubMed  Google Scholar 

  • Ménard A, Grillner S (2008) Diencephalic locomotor region in the lamprey–afferents and efferent control. J Neurophysiol 100:1343–1353

    Article  PubMed  Google Scholar 

  • Mezler M, Fleischer J, Conzelmann S, Korchi A, Widmayer P, Breer H, Boekhoff I (2001) Identification of a nonmammalian Golf subtype: functional role in olfactory signaling of airborne odorants in Xenopus laevis. J Comp Neurol 439:400–410

    Article  CAS  PubMed  Google Scholar 

  • Milner KL, Mogenson GJ (1988) Electrical and chemical activation of the mesencephalic and subthalamic locomotor regions in freely moving rats. Brain Res 452:273–285

    Article  CAS  PubMed  Google Scholar 

  • Miyasaka N, Arganda-Carreras I, Wakisaka N, Masuda M, Sümbül U, Seung HS, Yoshihara Y (2014) Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling. Nat Commun 5:3639

    Article  PubMed  Google Scholar 

  • Munger SD, Leinders-Zufall T, Zufall F (2009) Subsystem organization of the mammalian sense of smell. Annu Rev Physiol 71:115–140

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys R (1977) The brain of the lamprey in a comparative perspective. Ann N Y Acad Sci 299:97–145

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG, Puzdrowski RL (1988) Projections of the olfactory bulb and nervus terminalis in the silver lamprey. Brain Behav Evol 32:96–107

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG (2011) Olfactory projections in the white sturgeon, Acipenser transmontanus: an experimental study. J Comp Neurol 519:1999–2022

    Article  PubMed  Google Scholar 

  • Northcutt RG, Rink E (2012) Olfactory projections in the lepidosirenid lungfishes. Brain Behav Evol 79:4–25

    Article  PubMed  Google Scholar 

  • Ocaña FM, Suryanarayana SM, Saitoh K, Kardamakis AA, Capantini L, Robertson B, Grillner S (2015) The lamprey pallium provides a blueprint of the mammalian motor projections from cortex. Curr Biol 25:413–423

    Article  PubMed  Google Scholar 

  • Ohta Y, Grillner S (1989) Monosynaptic excitatory amino acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. J Neurophysiol 62:1079–1089

    Article  CAS  PubMed  Google Scholar 

  • Parker SM, Sinnamon HM (1983) Forward locomotion elicited by electrical stimulation in the diencephalon and mesencephalon of the awake rat. Physiol Behav 31:581–587

    CAS  PubMed  Google Scholar 

  • Pérez-Fernández J (2013) Characterization of Y and dopamine receptors in lampreys by using in situ hybridization: an evolutionary approach. PhD thesis, Functional Biology and Health Sciences, Universidad de Vigo

  • Pérez-Fernández J, Stephenson-Jones M, Suryanarayana SM, Robertson B, Grillner S (2014) Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression. J Comp Neurol 522:3775–3794

    Article  PubMed  Google Scholar 

  • Perret C, Millanvoye M, Cabelguen JM (1972) Ascending spinal messages during fictitious locomotion in curarized cats. J Physiol (Paris) 65:153A

    Google Scholar 

  • Pierre J, Repérant J, Ward R, Vesselkin NP, Rio JP, Miceli D, Kratskin I (1992) The serotoninergic system of the brain of the lamprey, Lampetra fluviatilis: an evolutionary perspective. J Chem Neuroanat 5:195–219

    Article  CAS  PubMed  Google Scholar 

  • Pierre J, Mahouche M, Suderevskaya EI, Repérant J, Ward R (1997) Immunocytochemical localization of dopamine and its synthetic enzymes in the central nervous system of the lamprey Lampetra fluviatilis. J Comp Neurol 380:119–135

    Article  CAS  PubMed  Google Scholar 

  • Polenova OA, Vesselkin NP (1993) Olfactory and nonolfactory projections in the river lamprey (Lampetra fluviatilis) telencephalon. J Hirnforsch 34:261–279

    CAS  PubMed  Google Scholar 

  • Pombal MA, El Manira A, Grillner S (1997) Afferents of the lamprey striatum with special reference to the dopaminergic system: a combined tracing and immunohistochemical study. J Comp Neurol 386:71–91

    Article  CAS  PubMed  Google Scholar 

  • Ren X, Chang S, Laframboise AJ, Green WW, Dubuc R, Zielinski BS (2009) Projections from the accessory olfactory organ into the medial region of the olfactory bulb in the sea lamprey (Petromyzon marinus): a novel vertebrate sensory structure? J Comp Neurol 516:105–116

    Article  PubMed  Google Scholar 

  • Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316–330

    Article  CAS  PubMed  Google Scholar 

  • Robertson B, Kardamakis AA, Capantini L, Pérez-Fernández J, Suryanarayana SM, Wallén P, Stephenson-Jones M, Grillner S (2014) The lamprey blueprint of the mammalian nervous system. Prog Brain Res 212:337–349

    Article  PubMed  Google Scholar 

  • Ryczko D, Dubuc R (2013) The multifunctional mesencephalic locomotor region. Curr Pharm Des 19:4448–4470

    Article  CAS  PubMed  Google Scholar 

  • Ryczko D, Grätsch S, Auclair F, Dubé C, Bergeron S, Alpert MH, Cone JJ, Roitman MF, Alford S, Dubuc R (2013) Forebrain dopamine neurons project down to a brainstem region controlling locomotion. Proc Natl Acad Sci 110:E3235-3242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryczko D, Cone JJ, Alpert MH, Goetz L, Auclair F, Dubé C, Parent M, Roitman MF, Alford S, Dubuc R (2016) A descending dopamine pathway conserved from basal vertebrates to mammals. Proc Natl Acad Sci 113:E2440-2449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryczko D, Grätsch S, Schläger L, Keuyalian A, Boukhatem Z, Garcia C, Auclair F, Büschges A, Dubuc R (2017) Nigral glutamatergic neurons control the speed of locomotion. J Neurosci 37:9759–9770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryczko D, Dubuc R (2017) Dopamine and the brainstem locomotor networks: From lamprey to human. Front Neurosci 11:295

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryczko D, Grätsch S, Alpert MH, Cone JJ, Kasemir J, Ruthe A, Beauséjour PA, Auclair F, Roitman MF, Alford S, Dubuc R (2020) Descending dopaminergic inputs to reticulospinal neurons promote locomotor movements. J Neurosci 40:8478–8490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salas CA, Yopak KE, Warrington RE, Hart NS, Potter IC, Collin SP (2015) Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis. Front Neurosci 9:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwanzel-Fukuda M, Morrell JI, Pfaff DW (1984) Localization of forebrain neurons which project directly to the medulla and spinal cord of the rat by retrograde tracing with wheat germ agglutinin. J Comp Neurol 226:1–20

    Article  CAS  PubMed  Google Scholar 

  • Scott WB (1896) Notes on the development of Petromyzon. J Morphol 1:253–310

    Article  Google Scholar 

  • Shik ML, Severin FV, Orlovskiĭ GN (1966) Control of walking and running by means of electric stimulation of the midbrain. Biofizika 11:659–666

    CAS  PubMed  Google Scholar 

  • Siefkes MJ, Winterstein SR, Li W (2005) Evidence that 3-keto petromyzonol sulphate specifically attracts ovulating female sea lamprey, Petromyzon marinus. Anim Behav 70:1037–1045

    Article  Google Scholar 

  • Sinnamon HM (1993) Preoptic and hypothalamic neurons and the initiation of locomotion in the anesthetized rat. Prog Neurobiol 41:323–344

    Article  CAS  PubMed  Google Scholar 

  • Sirota MG, Viana Di Prisco G, Dubuc R (2000) Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys. Eur J Neurosci 12:4081–4092

    Article  CAS  PubMed  Google Scholar 

  • Smetana RW, Alford S, Dubuc R (2007) Muscarinic receptor activation elicits sustained, recurring depolarizations in reticulospinal neurons. J Neurophysiol 97:3181–3192

    Article  CAS  PubMed  Google Scholar 

  • Smetana RW, Juvin L, Dubuc R, Alford S (2010) A parallel cholinergic brainstem pathway for enhancing locomotor drive. Nat Neurosci 13:731–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephenson-Jones M, Kardamakis AA, Robertson B, Grillner S (2013) Independent circuits in the basal ganglia for the evaluation and selection of actions. Proc Natl Acad Sci 110:E3670-3679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez R, García-González D, de Castro F (2012) Mutual influences between the main olfactory and vomeronasal systems in development and evolution. Front Neuroanat 6:50

    Article  PubMed  PubMed Central  Google Scholar 

  • Suryanarayana SM, Robertson B, Wallén P, Grillner S (2017) The lamprey pallium provides a blueprint of the mammalian layered cortex. Curr Biol 27:3264–3277

    Article  CAS  PubMed  Google Scholar 

  • Suryanarayana SM (2019) On the evolutionary origin of the vertebrate cortex. PhD thesis, Inst för neurovetenskap, Karolinska Institutet

  • Suryanarayana SM, Pérez-Fernández J, Robertson B, Grillner S (2020) The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nat Ecol Evol 4:639–651

    Article  PubMed  Google Scholar 

  • Suryanarayana SM, Pérez-Fernández J, Robertson B, Grillner S (2021a) The lamprey forebrain - evolutionary implications. Brain Behav Evol 1–16

  • Suryanarayana SM, Pérez-Fernández J, Robertson B, Grillner S (2021b) Olfaction in lamprey pallium revisited-Dual projections of mitral and tufted cells. Cell Rep 34:108596

  • Viala D, Buser P (1971) Methods of obtaining locomotor rhythms in the spinal rabbit by pharmacological treatments (DOPA, 5-HTP, D-amphetamine). Brain Res 35:151–165

    Article  CAS  PubMed  Google Scholar 

  • von Bartheld CS (2004) The terminal nerve and its relation with extrabulbar “olfactory” projections: lessons from lampreys and lungfishes. Microsc Res Tech 65:13–24

    Article  Google Scholar 

  • von Frisch K (1941) Über einen schreckstoff der fischhaut und seine biologische bedeutung. Z Vgl Physiol 29:46–145

    Article  Google Scholar 

  • Wagner CM, Stroud EM, Meckley TD (2011) A deathly odor suggests a new sustainable tool for controlling a costly invasive species. Can J Fish Aquat Sci 68:1157–1160

    Article  Google Scholar 

  • Weiss L, Jungblut LD, Pozzi AG, Zielinski BS, O’Connell LA, Hassenklöver T, Manzini I (2020) Multi-glomerular projection of single olfactory receptor neurons is conserved among amphibians. J Comp Neurol 528:2239–2253

    Article  PubMed  PubMed Central  Google Scholar 

  • Wickelgren WO (1977a) Physiological and anatomical characteristics of reticulospinal neurones in lamprey. J Physiol 270:89–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickelgren WO (1977b) Post-tetanic potentiation, habituation and facilitation of synaptic potentials in reticulospinal neurones of lamprey. J Physiol 270:115–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Zhang Q, Dexheimer TS, Ren J, Neubig RR, Li W (2020) Two highly related odorant receptors specifically detect alpha-bile acid pheromones in sea lamprey (Petromyzon marinus). J Biol Chem 295:12153–12166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zielinski BS, Moretti N, Hua HN, Zaidi AU, Bisaillon AD (2000) Serotonergic nerve fibers in the primary olfactory pathway of the larval sea lamprey, Petromyzon marinus. J Comp Neurol 420:324–334

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Mr. François Auclair for graphical assistance and Ms. Danielle Veilleux for technical assistance.

Funding

This work was supported by the Great Lakes Fishery Commission, Grants #54021, 54035, and 54067 to BZ and RD; the Canadian Institutes of Health Research, Grant #15129 to RD; the Natural Sciences and Engineering Research Council of Canada, Grants # 217435-01 to RD and 03916-2014 to BZ; PAB was supported by scholarships from the Natural Sciences and Engineering Research Council of Canada; the Fonds de Recherche du Québec- Santé; and Université de Montréal - Études supérieures et postdoctorales.

Author information

Authors and Affiliations

Authors

Contributions

The first draft of the manuscript was written by PAB and all authors commented on the manuscript. The authors read and approved the final manuscript.

Corresponding author

Correspondence to Réjean Dubuc.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beauséjour, PA., Zielinski, B. & Dubuc, R. Olfactory-induced locomotion in lampreys. Cell Tissue Res 387, 13–27 (2022). https://doi.org/10.1007/s00441-021-03536-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-021-03536-2

Keywords

Navigation