Skip to main content
SpringerLink
Log in

cGMP-Dependent Protein Kinase as a Modifier of Behaviour

  • Chapter
cGMP: Generators, Effectors and Therapeutic Implications

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 191))

Abstract

The importance of cGMP-dependent protein kinase (PKG) to the modulation of behavioural phenotypes has become increasingly clear in recent decades. The effects of PKG on behaviour have been studied in diverse taxa from perspectives as varied as ethology, evolution, genetics and neuropharmacology. The genetic variation of the Drosophila melanogaster gene, foraging (for), has provided a fertile model for examining natural variation in a single major gene influencing behaviour. Concurrent studies in other invertebrates and mammals suggest that PKG is an important signalling molecule with varied influences on behaviour and a large degree of pleiotropy and plasticity. Comparing these cross-taxa effects suggests that there are several potentially overlapping behavioural modalities in which PKG signalling acts to influence behaviours which include feeding, learning, stress and biological rhythms. More in-depth comparative analyses across taxa of the similarities and differences of the influence of PKG on behaviour may provide powerful mechanistic explications of the evolution of behaviour.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agostino PV, Plano SA, Golombek DA (2007) Sildenafil accelerates reentrainment of circadian rhythms after advancing light schedules. Proc Natl Acad Sci 104:9834–9839

    Article  PubMed  CAS  Google Scholar 

  • Arancio O, Antonova I, Gambaryan S, Lohmann SM, Wood JS, Lawrence DS, Hawkins RD (2001) Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation. J Neurosci 21:143–149

    PubMed  CAS  Google Scholar 

  • Bauer SJ, Sokolowksi MB (1985) A genetic analysis of path length and pupation height in a natural population of Drosophila melanogaster. Can J Gen Cyt 27:334–340

    Google Scholar 

  • Belay AT, Scheiner R, So AK-C, Douglas SJ, Chakabroty-Chatterjee M, Levine JD, Sokolowski MB (2007) The foraging gene of Drosophila melanogaster: spatial-expression analysis and sucrose responsiveness. J Comp Neurol 504:570–582

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE (2002) Influence of gene action across different time scales on behavior. Science 296:741–744

    Article  Google Scholar 

  • Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE (2003) cGMP-dependent changes in phototaxis: A possible role for the foraging gene in honey bee division of labour. J Exp Biol 206:2507–2515

    Article  CAS  Google Scholar 

  • Beshers SN, Huang ZY, Oono Y, Robinson GE (2001) Social inhibition and the regulation of temporal polyethism in honey bees. J Theor Biol 213:461–479

    Article  PubMed  CAS  Google Scholar 

  • Boisvert MJ, Shery DF (2006) Interval timing by an invertebrate, the bumble bee Bombus impatiens. Curr Biol 16:1636–1640

    Article  PubMed  CAS  Google Scholar 

  • Bolshakov VY, Siegelbaum SA (1995) Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269:1730–1734

    Article  PubMed  CAS  Google Scholar 

  • Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581–609

    Article  PubMed  CAS  Google Scholar 

  • Castellucci VF, Kandel ER (1974) A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc Natl Acad Sci 71:5004–5008

    Article  PubMed  CAS  Google Scholar 

  • Challet E, Caldelas I, Graff C, Pevet P (2003) Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biol Chem 384:711–719

    Article  PubMed  CAS  Google Scholar 

  • Challet E (2007) Clock genes, circadian rhythms and food intake. Pathol Biol (Paris) 55:176–177

    CAS  Google Scholar 

  • Chen C, Tonegawa S (1997) Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu Rev Neurosci 20:157–184

    Article  PubMed  CAS  Google Scholar 

  • Clem RL, Celikel T, Barth AL (2007) Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319:101–104

    Article  CAS  Google Scholar 

  • Comolli J, Hastings JW (1999) Novel Effects on The Gonyaulax Circadian System Produced by the Protein Kinase Inhibitor Staurosporine. J Biol Rhythms 14:10–18

    Article  Google Scholar 

  • Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 14:2950–2961

    Article  PubMed  CAS  Google Scholar 

  • Daniels SA, Ailion M, Thomas JH, Sengupta P (2000) egl-4 acts through a transforming growth factor-β/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues. Genetics 156:123–141

    PubMed  CAS  Google Scholar 

  • Dawson-Scully K, Armstrong GAB, Kent C, Robertson RM, Sokolowski MB (2007) Natural variation in the thermotolerance of neural function and behavior due to a cGMP dependent protein kinase. PLoS ONE 2:e773

    Article  CAS  Google Scholar 

  • Dean AM, Thornton JW (2007) Mechanistic approaches to the study of evolution: the functional synthesis. Nat Rev Genet 8:675–688

    Article  PubMed  CAS  Google Scholar 

  • de Bono M, Bargmann C (1998) Natural variation in a neuropeptIDe V receptor homolog modifies social behaviour and food response in C. elegans. Cell 94:679–689

    Article  PubMed  Google Scholar 

  • Douglas SJ, Dawson-Scully K, Sokolowski MB (2005) The neurogenetics and evolution of food-related behaviours. Trends in Neurosci 28:644–652

    CAS  Google Scholar 

  • Dunlap JC, Loros JL, Decoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer Associates, Sunderland MA

    Google Scholar 

  • de Belle SJ, Sokolowski MB (1987) Heredity of rover/sitter: Alternative foraging strategies of Drosophila melanogaster larvae. Heredity 59:73–83

    Article  Google Scholar 

  • de Belle SJ, Sokolowski MB (1989) Rover/sitter foraging behavior in Drosophila melanogaster: Genetic localization to chromosome-2L using compound autosomes. J Insect Behav 2:291–299

    Article  Google Scholar 

  • de Belle JS, Hilliker AJ, Sokolowski MB (1989) Genetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster. Genetics 123:157–163

    PubMed  Google Scholar 

  • de Belle JS, Sokolowski MB, Hilliker AJ (1993) Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36:94–101

    Article  PubMed  Google Scholar 

  • Engel JE, Wu C-F (1996) Alteration of non-associative conditioning of an IDentified escape circuit in Drosophila memory mutants. J Neurosci 16:3486–3499

    PubMed  CAS  Google Scholar 

  • Engel JE, Xie X-J, Sokolowski MB, Wu C-F (2000) A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant-fiber escape circuit in Drosophila. Learn Mem 7:341–352

    Article  PubMed  CAS  Google Scholar 

  • L'Etoile N, Coburn C, Kistler A, Gallegos G, Bargmann C (2002) The cyclic GMP-dependent protein kinase EGL-4 directs olfactory adaptation in C. elegans. Neuron 36:1079–1089

    Article  PubMed  Google Scholar 

  • Feil R, Hartmann J, Luo C, Wolfsgruber W, Schilling K, Feil S, Barski JJ, Meyer M, Konnerth A, De Zeeuw CI, Hofmann F (2003) Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I. J Cell Biol 163:295–302

    Article  PubMed  CAS  Google Scholar 

  • Feil R, Hofmann F, Kleppisch T (2005) Function of cGMP-dependent protein kinases in the nervous system. Rev Neurosci 16:23–41

    PubMed  CAS  Google Scholar 

  • Feil R, Kleppisch T (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol. 2008:529–560

    Article  Google Scholar 

  • Fitzpatrick MJ, Sokolowski MB (2004) In search of food: Exploring the evolutionary link between cGMP-dependent protein kinase (PKG) and behaviour. Int Comp Biol 44:28–36

    Article  CAS  Google Scholar 

  • Fitzpatrick MJ, Feder E, Rowe L, Sokolowski MB (2007) Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447:210–212

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara M, Sengupta P, McIntire SL (2002) Regulation of body size and behavioral state of C. elegans by sensory perception and EGL-4 cGMP-dependent protein kinase. Neuron 36:1091–1102

    Article  PubMed  CAS  Google Scholar 

  • Golombek DA, Agostino PV, Plano SA, Ferreyra GA (2004) Signalling in the mammalian circa-dian clock: the NO/cGMP pathway. Neurochem Int 45:929–936

    Article  PubMed  CAS  Google Scholar 

  • Graf SA, Sokolowski MB (1989) Rover/sitter Drosophila melanogaster larval foraging polymorphism as a function of larval development, food-patch quality, and starvation. J Insec Behav 2:301–313

    Article  Google Scholar 

  • Hawkins RD, Kandel ER, Bailey CH (2006) Molecular Mechanisms of Memory Storage in Aplysia. Biol Bull 210:174–191

    Article  PubMed  CAS  Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4: 266–275

    Article  PubMed  CAS  Google Scholar 

  • Hirose T, Nakano Y, Nagamatsu Y, Misumi T, Ohta H, Ohshima Y (2003) Cyclic GMP-dependent protein kinase EGL-4 controls body size and lifespan in C. elegans. Development 130: 1089–1099

    Article  PubMed  CAS  Google Scholar 

  • Hofmann F, Feil R, Kleppisch T, Schlossmann J (2006) Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 86:1–23

    Article  PubMed  CAS  Google Scholar 

  • Horikawa K, Minami Y, Iijima M, Akiyama M, Shibata S (2005) RapID damping of food-entrained circadian rhythm of clock gene expression in clock-defective peripheral tissues under fasting conditions. Neuroscience 134:335–343

    Article  PubMed  CAS  Google Scholar 

  • Ingram KK, Oefner P, Gordon DM (2005) Task-specific expression of the foraging gene in harvester ants. Mol Ecol 14:813–818

    Article  PubMed  CAS  Google Scholar 

  • Jouvert P, Revel MO, Lazaris A, Aunis D, Langley K, Zwiller J (2004) Activation of the cGMP pathway in dopaminergic structures reduces cocaine-induced EGR-1 expression and locomotor activity. J Neurosci 24:10716

    Article  PubMed  CAS  Google Scholar 

  • Kaun KR, Riedl CAL, Chakaborty-Chatterjee M, Belay AT, Douglas SJ, Gibbs AG, Sokolowski MB (2007a) Natural variation in food acquisition mediated via a Drosophila cGMP-dependent protein kinase. J Exp Biol 210:3547–3558

    Article  CAS  Google Scholar 

  • Kaun KR, Hendel T, Gerber B, Sokolowski MB (2007b) Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn Mem 14: 342–349

    Article  Google Scholar 

  • Kleppisch T, Pfeifer A, Klatt P, Ruth P, Montkowski A, Fassler R, Hofmann F (1999) Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxIDe synthase. J Neurosci 19:48–55

    PubMed  CAS  Google Scholar 

  • Kleppisch T, Wolfsgruber W, Feil S, Allmann R, Wotjak CT, Goebbels S, Nave K-A, Hofmann F, Feil R (2003) Hippocampal cyclic GMP-dependent protein kinase I supports an age- and protein synthesis dependent component of long-term potentiation but is not essential for spatial reference and contextual memory. J Neurosci 23:6005–6012

    PubMed  CAS  Google Scholar 

  • Lee G, Bahn JH, Park JH (2006) Sex- and clock-controlled expression of the neuropeptIDe F gene in Drosophila. Proc Natl Acad Sci 103:12580–12585

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Wolf R, Ernst R, Heisenberg M (1999) Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400:753–756

    Article  PubMed  CAS  Google Scholar 

  • Mackay TFC (2004) The genetic architecture of quantitative traits: lessons from Drosophila. Curr Opin Genet Dev 14:253–257

    Article  PubMed  CAS  Google Scholar 

  • Mathur A, Golombek DA, Ralph MR (1996) cGMP-dependent protein kinase inhibitors block light-induced phase advances of circadian rhythms in vivo. Am J Physiol Regul Integr Comp Physiol 270:R1031–R1036

    CAS  Google Scholar 

  • Mendoza J, Graff C, Dardente H, Pevet P, Challet E (2005) Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J Neurosci 25:1514–1522

    Article  PubMed  CAS  Google Scholar 

  • Mery F, Belay AT, So AK-C, Sokolowski MB, Kawecki TJ (2007) Natural polymorphism affecting learning and memory in Drosophila. Proc Natl Acad Sci 104:13051–13055

    Article  PubMed  CAS  Google Scholar 

  • Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8:845–856

    Article  CAS  Google Scholar 

  • Newman AEM, Foerster M, Shoemaker KL, Robertson RM (2003) Stress-induced thermotolerance of ventilatory motor pattern generation in the locust, Locusta migratoria. J Insect Physiol 49:1039–1047

    Article  PubMed  CAS  Google Scholar 

  • Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB (1997) Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834–836

    Article  PubMed  CAS  Google Scholar 

  • Osborne KA, de Belle JS, Sokolowski MB (2001) Foraging behaviour in Drosophila larvae: mushroom body ablation. Chem Senses 26:223–230

    Article  PubMed  CAS  Google Scholar 

  • Oster H, Werner C, Magnone MC, Mayser H, Feil R, Seeliger MW, Hofmann F, Albrecht U (2003) cGMP-dependent protein kinase II modulates mPer1 and mPer2 gene induction and influences phase shifts of the circadian clock. Curr Biol 13:725–733

    Article  PubMed  CAS  Google Scholar 

  • Pereira HS, Sokolowski MB (1993) Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc Natl Acad Sci 90:5044–5046

    Article  PubMed  CAS  Google Scholar 

  • Pereira HS, MacDonald DE, Hilliker AJ, Sokolowski MB (1995) Chaser (Csr), a new gene affecting larval foraging behaviour in Drosophila melanogaster. Genetics 141:263–270

    PubMed  CAS  Google Scholar 

  • Prasad NG, Shakarad M, Anitha D, Rajamani M, Joshi A (2001) Correlated responses to selection for faster development and early reproduction in Drosophila: the evolution of larval traits. Evolution 55:1363–1372

    PubMed  CAS  Google Scholar 

  • Raizen DM, Cullison KM, Pack AI, Sundaram MV (2006) A novel gain-of-function mutant of the cyclic GMP-dependent protein kinase egl-4 affects multiple physiological processes in Caenorhabditis elegans. Genetics 173:177–187

    Article  PubMed  CAS  Google Scholar 

  • Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV, Pack AI (2008) Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451:569–572

    Article  PubMed  CAS  Google Scholar 

  • Ramirez JM, Elsen FP, Robertson RM (1999) Long-term effects of prior heat shock on neuronal potassium currents recorded in a novel insect ganglion slice preparation. J Neurophysiol 81:795–802

    PubMed  CAS  Google Scholar 

  • Riedl CAL, Neal SJ, Robichon A, Westwood JT, Sokolowski MB (2005) Drosophila soluble guanylyl cyclase mutants exhibit increased foraging locomotion: behavioral and genomic investigations. Behav Gen 35:231–244

    Article  Google Scholar 

  • Renger JJ, Yao WD, Sokolowski MB, Wu CF (1999) Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. J Neurosci 19:RC28

    PubMed  CAS  Google Scholar 

  • Rodriguez L, Sokolowski MB, Shore JS (1992) Habitat selection by Drosophila melanogaster larvae. J Evol Biol 5:61–70

    Article  Google Scholar 

  • Sarov-Blat L, So WV, Liu L, Rosbash M (2000) The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 101:647–656

    Article  Google Scholar 

  • Sewell D, Burnet B, Connolly K (1975) Genetic analysis of larval feeding behavior in Drosophila melanogaster. Genet Res Cambr 24:163–173

    Article  Google Scholar 

  • Shettleworth SJ (2001) Animal cognition and animal behaviour. Anim Behav 61:277–286

    Article  Google Scholar 

  • Scheiner R, Barnert M, Erber J (2003) Variation in water and sucrose responsiveness during the foraging season affects proboscis extension learning in honey bees. ApIDologie 34:67–72

    Article  Google Scholar 

  • Scheiner R, Sokolowski MB, Erber J (2004) Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn Mem 11: 303–311

    Article  PubMed  Google Scholar 

  • SchmIDt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG (2002) cGMP-mediated signalling via cGKIalpha is required for the guIDance and connectivity of sensory axons. J Cell Biol 159:489–498

    Article  PubMed  CAS  Google Scholar 

  • Shaver SA, Varnam CJ, Hilliker AJ, Sokolowski MB (1998) The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behav Brain Res 95:23–29

    Article  PubMed  CAS  Google Scholar 

  • Shaver SA, Riedl CAL, Parkes TL, Sokolowski MB, Hilliker AJ (2000) Isolation of larval behavioural mutants in Drosophila melanogaster. J. Neurogenet. 14:193–205

    Article  PubMed  CAS  Google Scholar 

  • Sokolowski MB (1980) Foraging strategies of Drosophila melanogaster: a chromosomal analysis. Behav Genet 10:291–302

    Article  PubMed  CAS  Google Scholar 

  • Sokolowski MB (1982) Rover and sitter larval foraging patterns in a natural population of Drosophila melanogaster. Dros Inf Serv 58:130–139

    Google Scholar 

  • Sokolowski MB, Kent C, Wong J (1984) Drosophila larval foraging behaviour: developmental stages. Anim Behav 32:645–651

    Article  Google Scholar 

  • Sokolowski MB (1986) Ecological genetics and behaviour of Drosophila melanogaster larvae in nature. Anim Behav 34:403–408

    Article  Google Scholar 

  • Sokolowski MB (1987) Drosophila larval foraging behavior and correlated behaviors. In: Heuttel MD (ed.) Evolutionary genetics of invertebrate behavior. Plenum, NY, pp 197–213

    Google Scholar 

  • Sokolowski MB, Carton Y (1989) Microgeographic variation in Drosophila melanogaster larval behavior. J Insect Behav 2:138–139

    Article  Google Scholar 

  • Sokolowski MB, Pereira HS, Hughes K (1997) Evolution of foraging behavior in Drosophila by density-dependent selection. Proc Natl Acad Sci 94:7373–7377

    Article  PubMed  CAS  Google Scholar 

  • Stamps JA, Buechner M, Alezander K, Davis J, Zuniga N (2005) Genotypic differences in space use and movement patterns in Drosophila melangoaster. Anim Behav 70:609–618

    Article  Google Scholar 

  • Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852–1861

    PubMed  CAS  Google Scholar 

  • Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291:490–493

    Article  PubMed  CAS  Google Scholar 

  • Tegeder I, SchmIDtko A, Niederberger E, Ruth P, Geisslinger G (2002) Dual effects of spinally delivered 8-bromo-cyclic guanosine mono-phosphate (8-bromo-cGMP) in formalin-induced no-ciception in rats. Neurosci Lett 332:146–150

    Article  PubMed  CAS  Google Scholar 

  • Tegeder I, Del Turco D, SchmIDtko A, Sausbier M, Feil R, Hofmann F, Deller T, Ruth P, and Geisslinger G (2004) Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Natl Acad Sci 101: 3253–3257

    Article  PubMed  CAS  Google Scholar 

  • Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43

    Article  PubMed  CAS  Google Scholar 

  • Tischkau SA, Weber ET, Abbott SM, Mitchell JW, and Gillette MU (2003) Circadian clock-controlled regulation of cGMP-protein kinase G in the nocturnal domain. J Neurosci 23: 7543–7550

    PubMed  CAS  Google Scholar 

  • Tischkau SA, Mitchell JW, Pace LA, Barnes JW, Barnes JA, and Gillette MU (2004) Protein kinase G type II is required for night-to-day progression of the mammalian circadian clock. Neuron 43:539–549

    Article  PubMed  CAS  Google Scholar 

  • Toth AL, Robinson GE (2007) Evo-devo and the evolution of social behavior. Trends Genet 23:334–341

    Article  PubMed  CAS  Google Scholar 

  • Varnam CJ, Strauss R, de Belle JS, Sokolowski MB (1996) Larval behaviour of central complex mutants in Drosophila melanogaster: interactions between no brIDge, foraging and Chaser. J Neurogenetic 11:99–115

    Article  CAS  Google Scholar 

  • Vivancos GG, Parada CA, and Ferreira SH (2003) Opposite nociceptive effects of the arginine/NO/cGMP pathway stimulation in dermal and subcutaneous tissues. Br J Pharmacol 138:1351–1357

    Article  PubMed  CAS  Google Scholar 

  • Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nat Rev Genet 8:921–931

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Robinson PJ (1997) Cyclic GMP-dependent protein kinase and cellular signalling in the nervous system. J. Neurochem 68:443–456

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Pan Y, Li W, Jiang H, Chatzimanolis L, Chang J, Gong Z, Liu L (2008) Visual pattern memory requires foraging function in the central complex of Drosophila. Learn Mem 15: 133–142

    Article  PubMed  CAS  Google Scholar 

  • Werner C, Raivich G, Cowen M, Strekalova T, Sillaber I, Buters JT, Spanagel R, Hofmann F (2004) Importance of NO/cGMP signalling via cGMP-dependent protein kinase II for controlling emotionality and neurobehavioural effects of alcohol. Eur J Neurosci 20:3498–3506

    Article  PubMed  Google Scholar 

  • Wu CL, Xia S, Fu TF, Wang H, Chen YH, Leong D, Chiang AS, Tully T (2007) Specific requirement of NMDA receptors for long-term memory consolIDation in Drosophila ellipsoID body. Nat Neurosci 10:1578–1586

    Article  PubMed  CAS  Google Scholar 

  • Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994) Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635–639

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Toronto, Mississauga, ON, L5L1C6, Canada

    Christopher J. Reaume & Marla B. Sokolowski

Authors
  1. Christopher J. Reaume
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marla B. Sokolowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marla B. Sokolowski .

Editor information

Editors and Affiliations

  1. Dept. Pharmacology, Monash University, Wellington Road, Clayton, VIC, 3800, Australia

    Harald H. H. W. Schmidt

  2. Inst. Pharmakologie und Toxikologie, TU München, Biedersteiner Str. 29, München, 80802, Germany

    Franz Hofmann

  3. Bayer Schering Pharma AG Cardiology Research, Pharma Research Center, Wuppertal, 42096, Germany

    Johannes-Peter Stasch

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer

About this chapter

Cite this chapter

Reaume, C.J., Sokolowski, M.B. (2009). cGMP-Dependent Protein Kinase as a Modifier of Behaviour. In: Schmidt, H.H.H.W., Hofmann, F., Stasch, JP. (eds) cGMP: Generators, Effectors and Therapeutic Implications. Handbook of Experimental Pharmacology, vol 191. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-68964-5_18

Download citation

Publish with us

Policies and ethics

Search

Navigation