Transcriptional control of behavior: Engrailed knock-out changes cockroach escape trajectories

Journal of Neuroscience

Volumn 29, Issue 22, 2009, Pages 7181-7190

  Booth, David ^a   Marie, Bruno ^b   Domenici, Paolo ^c   Blagburn, Jonathan M ^b   Bacon, Jonathan P ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENGRAILED PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BEHAVIOR CONTROL; COCKROACH; CONTROLLED STUDY; DIRECTIONAL VISION; ESCAPE BEHAVIOR; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; STIMULUS; SYNAPTIC POTENTIAL; THREAT; VISION; VISUAL STIMULATION;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; COCKROACHES; COMPUTER SIMULATION; ESCAPE REACTION; GANGLIA, INVERTEBRATE; HOMEODOMAIN PROTEINS; MODELS, BIOLOGICAL; PHYSICAL STIMULATION; PROBABILITY; RNA, DOUBLE-STRANDED; SENSORY RECEPTOR CELLS; SPATIAL BEHAVIOR; WIND;

EID: 66749084404     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1374-09.2009     Document Type: Article

References (46)

1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr AC-19:716-723.
2. Baader SL, Vogel MW, Sanlioglu S, Zhang X, Oberdick J (1999) Selective disruption of "late onset" sagittal banding patterns by ectopic expression of Engrailed-2 in cerebellar Purkinje cells. J Neurosci 19:5370-5379. (Pubitemid 29300203)
3. Batschelet E (1981) Circular statistics in biology. London: Academic.
4. Blagburn JM, Beadle DJ, Sattelle DB (1984) Synapses between an identified giant interneurone and a filiform hair sensory neurone in the terminal ganglion of first instar cockroaches (Periplaneta americana L.). J Exp Biol 113:477-481. (Pubitemid 15165722)
5. Blagburn JM, Gibbon CR, Bacon JP (1995) Expression of engrailed in an array of identified sensory neurons: comparison with position, axonal arborization, and synaptic connectivity. J Neurobiol 28:493-505.
6. Chen HH, Hippenmeyer S, Arber S, Frank E (2003) Development of the monosynaptic stretch reflex circuit. Curr Opin Neurobiol 13:96-102. (Pubitemid 36197933)
7. Clyne JD, Miesenböck G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133:354-363.
8. Comer CM, Dowd JP (1987) Escape turning behaviour of the cockroach. Changes in directionality induced by unilateral lesions of the abdominal nervous system. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 160:571-583.
9. Condron BG, Patel NH, Zinn K (1994) Engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system. Neuron 13:541-554. (Pubitemid 24300161)
10. Dagan D, Camhi JM (1979) Responses to wind recorded from the cercal nerve of the cockroach Periplaneta americana. II. Directional sensitivity of sensory axons innervating single columns of filiform hairs. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 133:103-111.
11. Dagan D, Volman SF (1982) Sensory basis for directional wind detection in first instar cockroaches, Periplaneta americana. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 147:471-478.
12. Domenici P (2002) Escape trajectory, ecological. In: Encyclopedia of environmetrics (El-Shaarawi AH, Piegorsch WW, eds), pp 708-711. Chichester, UK: Wiley.
13. Domenici P, Blake RW (1993) Escape trajectories in angelfish (Pterophyllum eimekei). J Exp Biol 177:253-272.
14. Domenici P, Booth D, Blagburn JM, Bacon JP (2008) Cockroaches keep predators guessing by using preferred escape trajectories. Curr Biol 18:1792-1796.
15. Ezrachi EA (2003) Computational model of the cockroach escape behavior: winner and losers in a population code. Biol Cybern 88:33-45.
16. Friedman GC, O'Leary DD (1996) Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J Neurosci 16:5498-5509.
17. Gymer A, Edwards JS (1967) The development of the insect nervous system. I. An analysis of postembryonic growth in the terminal ganglion of Acheta domesticus. J Morphol 123:191-197.
18. Heemskerk J, DiNardo S, Kostriken R, O'Farrell PH (1991) Multiple modes of engrailed regulation in the progression towards cell fate determination. Nature 352:404-410. (Pubitemid 21896730)
19. Hill ES, Blagburn JM (1998) Indirect synaptic inputs from filiform hair sensory neurons contribute to the receptive fields of giant interneurons in the first-instar cockroach. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 183:467-476. (Pubitemid 28514652)
20. Holman D (2003) mle: a programming language for building likelihood models. Version 2.1, Vol 1, User's manual. Vol 2, Reference manual. http://faculty.washington.edu/~djholman/mle.
21. Hurvich C, Tsai C (1989) Regression and time series model selection in small samples. Biometrika 78:499-509.
22. Joly W, Mugat B, Maschat F (2007) Engrailed controls the organization of the ventral nerve cord through frazzled regulation. Dev Biol 301:542-554. (Pubitemid 46073983)
23. Keegan AP, Comer CM (1993) The wind-elicited escape response of cockroaches (Periplaneta americana) is influenced by lesions rostral to the escape circuit. Brain Res 620:310-316.
24. Kolton L, Camhi JM (1995) Cartesian representation of stimulus direction: parallel processing by two sets of giant interneurons in the cockroach. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 176:691-702.
25. Levi R, Camhi JM (2000a) Population vector coding by the giant interneurons of the cockroach. J Neurosci 20:3822-3829. (Pubitemid 30266243)
26. Levi R, Camhi JM (2000b) Wind direction coding in the cockroach escape response: winner does not take all. J Neurosci 20:3814-3821. (Pubitemid 30266242)
27. Logan C, Wizenmann A, Drescher U, Monschau B, Bonhoeffer F, Lumsden A (1996) Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr Biol 6:1006-1014. (Pubitemid 26350721)
28. Lundell MJ, Chu-LaGraff Q, Doe CQ, Hirsh J (1996) The engrailed and huckebein genes are essential for development of serotonin neurons in the Drosophila CNS. Mol Cell Neurosci 7:46-61. (Pubitemid 26088259)
29. Marie B, Bacon JP (2000) Two engrailed-related genes in the cockroach: cloning, phylogenetic analysis, expression and isolation of splice variants. Dev Genes Evol 210:436-448.
30. Marie B, Blagburn JM (2003) Differential roles of Engrailed paralogs in determining sensory axon guidance and synaptic target recognition. J Neurosci 23:7854-7862. (Pubitemid 37052353)
31. Marie B, Bacon JP, Blagburn JM (2000) Double-stranded RNA interference shows that Engrailed controls the synaptic specificity of identified sensory neurons. Curr Biol 10:289-292. (Pubitemid 30152954)
32. Marie B, Cruz-Orengo L, Blagburn JM (2002) Persistent engrailed expression is required to determine sensory axon trajectory, branching, and target choice. J Neurosci 22:832-841.
33. Miller JP, Jacobs GA, Theunissen FE (1991) Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons. J Neurophysiol 66:1680-1689.
34. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795-801. (Pubitemid 11214475)
35. Nye SW, Ritzmann RE (1992) Motion analysis of leg joints associated with escape turns of the cockroach, Periplaneta americana. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 171:183-194.
36. Ritzmann RE, Pollack AJ (1988) Wind-activated thoracic interneurons of the cockroach. II. Patterns of connection from ventral giant interneurons. J Neurobiol 19:589-611.
37. Ritzmann RE, Pollack AJ (1990) Parallel motor pathways from thoracic interneurons of the ventral giant interneuron system of the cockroach, Periplaneta americana. J Neurobiol 21:1219-1235.
38. Saueressig H, Burrill J, Goulding M (1999) Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126:4201-4212. (Pubitemid 29509336)
39. Shimizu H, Shimoda M, Yamaguchi T, Seong KH, Okamura T, Ishii S (2008) Drosophila ATF-2 regulates sleep and locomotor activity in pacemaker neurons. Mol Cell Biol 28:6278-6289.
40. Siegler MV, Jia XX (1999) Engrailed negatively regulates the expression of cell adhesion molecules connectin and neuroglian in embryonic Drosophila nervous system. Neuron 22:265-276. (Pubitemid 29109661)
41. Stern M, Ediger VL, Gibbon CR, Blagburn JM, Bacon JP (1997) Regeneration of cercal filiform hair sensory neurons in the first-instar cockroach restores escape behavior. J Neurobiol 33:439-458. (Pubitemid 27411223)
42. Thompson KS, Blagburn JM, Gibbon CR, Bacon JP (1992) Correlation of filiform hair position with sensory afferent morphology and synaptic connections in the second instar cockroach. J Comp Neurol 320:213-227.
43. Von Stetina SE, Fox RM, Watkins KL, Starich TA, Shaw JE, Miller DM 3rd (2007) UNC-4 represses CEH-12/HB9 to specify synaptic inputs to VA motor neurons in C. elegans. Genes Dev 21:332-346.
44. Westin J, Langberg JJ, Camhi JM (1977) Responses of the giant interneurons of the cockroach Periplaneta americana to wind puffs of different directions and velocities. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 121:307-324.
45. Westin J, Ritzmann RE, Goddard DJ (1988) Wind-activated thoracic interneurons of the cockroach. I. Responses to controlled wind stimulation. J Neurobiol 19:573-588.
46. Yamamoto D (2008) Brain sex differences and function of the fruitless gene in Drosophila. J Neurogenet 15:1-24.