Schafer lab Papers

Research Articles on C. elegans Behaviour


Schwarz RF, Branicky R, Grundy LJ, Schafer WR, Brown AEX (2015), "Changes in postural syntax underlie sensory modulation and natural variation of C. elegans locomotion" PLoS Comp Biol 11: e1004322.

Choi S, Taylor KP, Chatzigeorgiou M, Hu Z, Schafer WR, Kaplan JM (2015) , "Sensory neurons arouse C. elegans locomotion via both glutamate and neuropeptide release.” PLoS Genetics 11: e1005359

Rabinowitch I, Schafer WR (2015), "Engineering new synaptic connections in C. elegans.” Worm Epub 28 Jan 2015

Schafer WR (2015), "Mechanosensory molecules and circuits in C. elegans.” Pflügers Arch. 467: 39-48.

Butler VJ, Branicky R, Yemini E, Liewald JF, Gottschalk A, Kerr RA, Chklovskii DB, Schafer WR (2015), “A consistent muscle activation strategy underlies crawling and swimming in Caenorhabditis elegans.” J R Soc Interface 12(102):20140963


Branicky R, Miyazaki H, Strange K, Schafer WR (2014), “The Voltage-Gated Anion Channels Encoded by clh-3 Regulate Egg Laying in C. elegans by Modulating Motor Neuron Excitability.” J Neurosci 34(3):764-75

Cohen E, Chatzigeorgiou M, Husson SJ, Steuer-Costa W, Gottschalk A, Schafer WR, Treinin M (2014), “Caenorhabditis elegans nicotinic acetylcholine receptors are required for nociception.” Mol Cell Neurosci

Pavlovic DM, Vértes PE, Bullmore ET, Schafer WR, Nichols TE (2014), “Stochastic Blockmodeling of the Modules and Core of the Caenorhabditis elegans Connectome.” PLoS One 9(7):e97584

Rabinowitch I, Chatzigeorgiou M, Zhao B, Treinin M, Schafer WR (2014), “Rewiring neural circuits by the insertion of ectopic electrical synapses in transgenic C. elegans.” Nat Commun 5:4442


Brown AE, Yemini EI, Grundy LJ, Jucikas T, Schafer WR (2013), “A dictionary of behavioral motifs reveals clusters of genes affecting Caenorhabditis elegans locomotion.” Proc Natl Acad Sci U S A 110(2):791-6

Chatzigeorgiou M, Bang S, Hwang SW, Schafer WR (2013), “tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans.” Nature

Choi S, Chatzigeorgiou M, Taylor KP, Schafer WR, Kaplan JM (2013), “Analysis of NPR-1 Reveals a Circuit Mechanism for Behavioral Quiescence in C. elegans.” Neuron 78(5):869-80

Nicosia V, Vértes PE, Schafer WR, Latora V, Bullmore ET (2013), “Phase transition in the economically modeled growth of a cellular nervous system.” Proc Natl Acad Sci U S A 110(19):7880-5

Rabinowitch I, Chatzigeorgiou M, Schafer WR (2013), “A gap junction circuit enhances processing of coincident mechanosensory inputs.” Curr Biol 23(11):963-7

Smith CJ, O'Brien T, Chatzigeorgiou M, Spencer WC, Feingold-Link E, Husson SJ, Hori S, Mitani S, Gottschalk A, Schafer WR, Miller DM 3rd (2013), “Sensory Neuron Fates Are Distinguished by a Transcriptional Switch that Regulates Dendrite Branch Stabilization.” Neuron 79(2):266-80

Towlson EK, Vértes PE, Ahnert SE, Schafer WR, Bullmore ET (2013), “The Rich Club of the C. elegans Neuronal Connectome.” J Neurosci 33(15):6380-6387

Yemini E, Jucikas T, Grundy LJ, Brown AE, Schafer WR (2013), “A database of Caenorhabditis elegans behavioral phenotypes.” Nat Methods 10(9):877-9


Cohen E, Yemini E, Schafer W, Feitelson DG, Treinin M (2012), “Locomotion analysis identifies roles of mechanosensory neurons in governing locomotion dynamics of C. elegans.” J Exp Biol 215(Pt 20):3639-48

Wen Q, Po MD, Hulme E, Chen S, Liu X, Kwok SW, Gershow M, Leifer AM, Butler V, Fang-Yen C, Kawano T, Schafer WR, Whitesides G, Wyart M, Chklovskii DB, Zhen M, Samuel AD (2012), “Proprioceptive coupling within motor neurons drives C. elegans forward locomotion.” Neuron 76(4):750-61


Yemini E, Kerr RA, Schafer WR (2011), “Preparation of samples for single-worm tracking.” Cold Spring Harb Protoc 2011(12):1475-9

Yemini E, Kerr RA, Schafer WR (2011), “Illumination for worm tracking and behavioral imaging.” Cold Spring Harb Protoc 2011(12):1480-2

Yemini E, Kerr RA, Schafer WR (2011), “Tracking movement behavior of multiple worms on food.” Cold Spring Harb Protoc 2011(12):1483-7

Aoki R, Yagami T, Sasakura H, Ogura K, Kajihara Y, Ibi M, Miyamae T, Nakamura F, Asakura T, Kanai Y, Misu Y, Iino Y, Ezcurra M, Schafer WR, Mori I, Goshima Y (2011), “A seven-transmembrane receptor that mediates avoidance response to dihydrocaffeic acid, a water-soluble repellent in Caenorhabditis elegans.” J Neurosci 31(46):16603-10

Chatzigeorgiou M, Schafer WR (2011) “Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans” Neuron 70: 299-309.

Ezcurra M, Tanizawa Y, Swoboda P, Schafer WR (2011) “Food sensitizes C. elegans avoidance behaviors through acute dopamine signaling” EMBO J 30: 1110-1122. Epub 8 Feb 2011.

Albeg A, Smith C, Chatzigeorgiou M, Feitelson D, Hall DH, Schafer WR, Miller DM, Treinin M (2011) “C. elegans multi-dendritic sensory neurons: morphology and function” Mol Cell Neurosci. 46: 308-317. Epub 2010 Oct 21.


Chatzigeorgiou M, Yoo S, Watson JD, Lee WH, Spencer C, Kindt KS, Hwang SW, Miller DM, Treinin M, Driscoll M, Schafer WR (2010) “Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors” Nature Neuosci. Epub 2010 May 30.

Chatzigeorgiou M, Grundy L, Kindt KS, Lee WH, Driscoll M, Schafer WR (2010) “Spatial asymmetry in the mechanosensory phenotypes of the C. elegans DEG/ENaC gene mec-10.” J. Neurophysiol. 104: 3334-3344. Epub 2010 Sep 29.

Albeg A, Smith C, Chatzigeorgiou M, Feitelson D, Hall DH, Schafer WR, Miller DM, Treinin M (2010) “C. elegans multi-dendritic sensory neurons: morphology and function” Mol Cell Neurosci. Epub 2010 Oct 21.

Kang L, Gao J, Schafer WR, Xie Z, Xu XZ (2010) “C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel.” Neuron 67: 381-91.

Zhang M, Schafer WR, Breitling R (2010) “A circuit model of the temporal pattern generator of Caenorhabditis egg-laying behavior” BMC Syst Biol 4: 81.

Ben Arous J, Tanizawa Y, Rabinowitch I, Chatenay D, Schafer WR (2010) “Automated imaging of neuronal activity in freely behaving Caenorhabditis elegans” J. Neurosci Meth 187: 229-34. Epub 2010 Jan 21.


Walker DS, Vázquez-Manrique RP, Gower NJD, Gregory E, Schafer WR, Baylis HA (2009) “Inositol 1,4,5-trisphosphate signalling regulates the avoidance response to nose touch in Caenorhabditis elegans” PLoS Genetics 5: e1000636 Epub 2009 Sep 4.

Senti G, Ezcurra M, Löbner J, Schafer WR, Swoboda P (2009) “Worms with a single functional sensory cilium generate proper neuron-specific behavioral output” Genetics 183: 595-605. Epub 2009 Aug 3.

Huang K-M, Cosman P, Schafer WR (2009) "Using articulated models for tracking multiple C. elegans in physical contact" J Sign Proc. Syst. 55: 113-126. Epub 2008 Jun 7.


Zhang M, Chung S, Fang-Yen C, Craig C, Kerr R, Suzuki H, Samuel A, Mazur E, Schafer WR (2008) "A self-regulating feed-forward circuit controlling C. elegans egg-laying behavior" Curr. Biol. 18: 1445-1455 Epub 2008 Sep 25.

Suzuki H, Thiele T, Faumont S, Ezcurra M, Lockery S, Schafer WR. (2008) "Functional asymmetry in C. elegans salt taste neurons and its computational role in chemotaxis behaviour" Nature 454: 114-117.

Wang Y, Apicella A Jr, Lee SK, Ezcurra M, Slone RD, Goldmit M, Schafer WR, Shaham S, Driscoll M, Bianchi L. (2008) "A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans." EMBO J. 27: 2388-2399 Epub 2008 Aug 14.

Tearle AW, Gravato-Nobre MJ, Schafer WR, Hodgkin J. (2008) "The C. elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis" Dev Biol 17: 549-59. Epub 2008 Mar 14.

Yeh E, Ng S, Zhang M, Bouhours M, Wang Y,, Wang M, Hung W, Aoyagi K, Melnik-Martinez K, Li M, Liu F, Schafer WR, Zhen M (2008) "A putative cation channel NCA-1 and a novel protein UNC-80 regulate synaptic activity in C. elegans" PLoS Biol. 6: e55.

Huang K-M, Cosman P, Schafer WR (2008) "Automated detection and analysis of foraging behavior in C. elegans" J. Neurosci Meth. 171: 153-164. Epub 2008 Feb 12.


Kindt KS, Quast KB, Giles AG, De S, Hendrey D, Nicastro I, Rankin CH, Schafer WR (2007) "Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans" Neuron 55: 662-676.

Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schafer WR (2007) “Caenorhabditis elegans TRPA-1 functions in mechanosensation.” Nature Neurosci 10: 568-577. Epub 2007 Apr 22.

Eimer S, Gottschalk A, Hengartner M, Horvitz HR, Richmond J, Schafer WR, Bessereau J-L (2007) "Regulation of nicotinic receptor trafficking by the transmembrane Golgi protein UNC-50" EMBO J 26: 4313-4323.

Ferkey DM, Hyde R, Haspel G, Dionne HM, Hess HA, Suzuki H, Schafer WR, Koelle MR, Hart AC (2007) “C. elegans G protein regulator RGS-3 controls sensitivity to sensory stimuli” Neuron 53: 39-52.


Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y (2006) "The insulin/PI3 –kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans" Neuron 51: 613-626

Frøkjær-Jensen C, Kindt KS, Kerr RA, Suzuki H, Melnik-Martinez K, Gerstbrein B, Driscoll M, Schafer WR (2006) "Effects of voltage-gated calcium channel subunit genes on calcium influx in cultured C. elegans mechanosensory neurons" J. Neurobiol. 66: 1125-1139 Epub 2006 Jul 11

Huang KM, Cosman P, Schafer WR. (2006) "Machine vision based detection of omega bends and reversals in C. elegans" J Neurosci Meth. 158: 323-336. Epub 2006 Jul 1

Gottschalk A, Schafer WR (2006) "Visualization of integral and peripheral cell surface proteins in live Caenorhabditis elegans" J Neurosci Meth. 154: 68-79 Epub 2006 Feb 6


Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, Schafer WR. (2005) "In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents" EMBO J 24: 63-72. Epub 2004 Dec 02. +erratum

Gottschalk A, Almedom, RB, Schedletzky T, Anderson AD, Yates JR III, Schafer WR (2005) "Identification and characterization of novel nicotinic receptor-associated proteins in Caenorhabditis elegans." EMBO J 24:2566-78. Epub 2005 Jun 30.

Geng W, Cosman P. Palm M, Schafer W. (2005) "C. elegans egg-laying detection and behavior study using image analysis" EURASIP J. App. Sig. Proc. 14 : 2229-2240.


McKay, Raizen D, Gottschalk A, Schafer WR, Avery L (2004) )"eat-2 and eat-18 are required for nicotinic neurotransmission in the C. elegans pharynx Genetics" 166: 161-169.

Kahn-Kirby AH, Dantzker JLM, Apicella AJ, Schafer WR, Browse J, Bargmann CI, Watts JL (2004)) "Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo" Cell 19: 889-900.

Fukuto HS, Ferkey DM, Apicella AJ, Lans H, Sharmeen T, Chen W, Lefkowitz RJ, Jansen G, Schafer WR, Hart AC. (2004) "G Protein-coupled receptor kinase function is essential for chemosensation in C. elegans" Neuron 42: 581-593.

Bianchi L, Gerstbrein B, Frøkjær-Jensen C, Royal DC, Mukherjee G, Royal MA, Xue J, Schafer WR, Driscoll M. (2004) "The neurotoxic MEC-4(d) DEG/ENaC sodium channel conducts calcium: implications for necrosis initiation" Nature Neurosci 7: 1337-1344

Sanyal S, Wintle RF, Kindt K, Nuttley WM, Arvan R, Fitzmaurice P, Bigras E, Merz D, Hebert TE, van der Kooy D, Schafer WR, Culotti JG and Van Tol HHM. (2004) "Dopamine modulates the plasticity of mechanosensory responses in C. elegans" EMBO J 23: 473-482.

Geng W, Cosman P, Berry CC, Feng Z, Schafer WR. (2004) "Automatic tracking, feature extraction and classification of C. elegans phenotypes" IEEE Trans Biomed. Eng 51: 1811-20.

Feng Z., Cronin CJ, Wittig JH Jr, Sternberg PW, Schafer WR. (2004) "An imaging system for standardized quantitative analysis of C. elegans behavior" BMC Bioinformatics 5: 115.


Suzuki H, Kerr R, Bianchi L, Frøkjær-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M, Schafer WR. (2003) "In vivo functional analysis of C. elegans mechanosensory neurons reveals a specific role for MEC-4 channels in the process of gentle touch transduction" Neuron 39: 1005-1017.

Shyn SI, Kerr R, Schafer WR. (2003) "Serotonin and Go modulate functional states of neurons and muscles involved in C. elegans egg-laying behavior" Curr. Biol. 13: 1910-1915.

Geng W, Cosman P, Baek J-H, Berry CC, Schafer WR. (2003) "Quantitative classification and natural clustering of C. elegans behavioral phenotypes" Genetics 165: 1117-1123.

Baek J-H, Cosman P, Feng Z, Silver J, Schafer WR (2002) "Using machine vision system to analyze and classify of C. elegans behavioral phenotypes quantitatively" J. Neurosci Meth. 118: 9-21.

Kindt KS, Tam T, Whiteman S, Schafer WR. (2002) "Serotonin promotes Go/Gq-mediated neuronal migration in Caenorhabditis elegans" Curr. Biol. 12: 1738-1747.

Hardaker, LA, Singer E, Kerr R, Zhou GT, Schafer WR. (2001) "Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditis elegans" J. Neurobiol. 49: 303-313.

Kim J, Poole DS, Waggoner LE, Kempf A, Ramirez DS, Treschow PA, Schafer WR (2001) “Genes affecting affecting the activity of nicotinic receptors involved in Caenorhabditis elegans egg-laying behavior” Genetics 157: 1599-1610.


Waggoner LE, Dickinson KA, Poole DS, Tabuse Y, Miwa J, Schafer WR. (2000) “Long-term nicotine adaptation in Caenorhabditis elegans involves PKC-dependent changes in nicotinic receptor abundance” J. Neurosci. 20: 8802-8811.

Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR. (2000) “Optical imaging of calcium transients in C. elegans neurons and pharyngeal muscle” Neuron 26: 583-594.

Tam T, Mathews E, Snutch T, Schafer WR (2000) “Voltage-gated calcium channels direct neuronal migration in Caenorhabditis elegans” Dev. Biol. 226: 104-117.

Waggoner LE , Hardaker LA, Golik S, Schafer WR. (2000) “Effect of a neuropeptide gene on behavioral states in Caenorhabditis elegans egg-laying”. Genetics 134: 1181-1192


Waggoner LE, Zhou GT, Schafer RW, Schafer WR. (1998) “Control of alternative behavioral states by serotonin in Caenorhabditis elegans” Neuron 21: 203-214.

Zhou GT, Schafer WR, Schafer RW. (1998) “A three-state biological point process model and its parameter estimation” IEEE Trans. Signal Process. 46: 2698-2707.

Schafer W, Sanchez BM, Kenyon CJ. (1996) "Genes affecting sensitivity to serotonin in Cenorhabditis elegans." Genetics 143: 1219-1230.

Schafer, WR, Kenyon C. (1995) "A calcium channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans." Nature 375: 73-78.

Pre-worm work:

Dimster-Denk, DF, Schafer WR, Rine J. (1995) "Control of RAS mRNA by the mevalonate pathway." Mol. Biol. Cell. 6: 59-70.

Schafer, WR, Trueblood CE, Yang C-C, Mayer MP, Rosenberg S, Poulter CD, Kim S-H, Rine J. (1990) "Enzymatic coupling of cholesterol intermediates to a mating pheromone precursor and to the Ras protein." Science 249: 1133-1139.

Finegold, AA, Schafer WR, Rine J, Whiteway M, Tamanoi F. (1990) "Common modifications of trimeric G-proteins and ras proteins: involvement of polyisoprenylation." Science 249: 165-168.

Thorsness M, Schafer W, D'Ari L, Rine J. (1989) "Positive and negative transcriptional control by heme of genes encoding HMG-CoA reductase in Saccharomyces cerevesiae." Mol. Cell. Biol. 9: 5702-5712.

Schafer, WR, Kim R, Sterne R, Thorner J, Kim S-H, Rine J. (1989) "Genetic and pharmacological suppression of oncogenic mutations in RAS genes of yeast and humans." Science 245: 379-385.

Ray, C., M. Igo, W. Schafer, R. Losick, C.P. Moran, Jr. (1988) "Suppression of ctc promoter mutations in Bacillus subtilis." J. Bacteriol. 170: 900-907.

Igo, M., M. Lampe, C. Ray, W. Schafer, C.P. Moran, Jr., R. Losick. (1987) "Genetic studies of a secondary RNA polymerase sigma factor in Bacillus subtilis." J. Bacteriol. 169: 3464-3469.

Reviews related to our work:

Schafer WR (2015), “Mechanosensory molecules and circuits in C. elegans.” Pflugers Arch

Schafer WR (2006) "Genetics of egg-laying in worms" Ann Rev Genet. 40: 487-509.

Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM. (2006) "Guidelines on nicotine dose selection for in vivo research". (2006) Psychopharmacology (Berl). Epub 2006 Aug 9

Schafer WR (2005) "Deciphering the neural and molecular mechanisms of C. elegans behavior" Curr. Biol. 15: R723-R729.

Schafer WR (2004) "Addiction research in a simple animal model: the nematode Caenorhabditis elegans" Neuropharmacology 47 supp 1: 123-131. Epub 2006 Aug 9.

Schafer, WR (2002) "Genetic analysis of nicotinic signaling in worms and flies" J. Neurobiol. 53: 535-541

Schafer, WR, Rine J. (1992) "Protein prenylation: genes, enzymes, targets, and functions." Ann Rev Genet 26: 209-37

Other reviews/commentaries:

Zhao B, Schafer WR (2013), “Neuropeptide signaling: from the gut.” Curr Biol 23(11):R481-3

Schafer WR (2012), “Tackling thermosensation with multidimensional phenotyping.” BMC Biol 10:91

Brown AE, Schafer WR (2011), “Unrestrained worms bridled by the light.” Nat Methods 8(2):129-30

Branicky R, Schafer WR. (2009) Tyramine: a new receptor and a new role at the synapse. Neuron. 62: 458-460.

Rabinowitch I, Schafer W (2008) "Neuronal remodeling on the evolutionary timescale" J Biol 7: 37.

Branicky RS, Schafer WR. (2008) "Oxygen homeostasis: how the worm adapts to variable oxygen levels." Curr Biol. 18: R559-560.

Schafer WR. (2006) "Proprioception: a channel for body sense in the worm." Curr Biol. 16: R509-511.

Schafer, WR. (2002) "PKG and the genetic analysis of behavioral phenotypes" Neuron 36: 991-993.

Schafer, WR (1999) “How do antidepressants work? prospects for genetic analysis of drug mechanisms” Cell 98: 551-554.