Supplementary Materials for · 3 Fig. S1. Frontal autofluorescent section of the brain of the fruit...
Transcript of Supplementary Materials for · 3 Fig. S1. Frontal autofluorescent section of the brain of the fruit...
www.sciencemag.org/cgi/content/full/340/6129/157/DC1
Supplementary Materials for
Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia
Nicholas J. Strausfeld* and Frank Hirth*
*Corresponding author. E-mail: [email protected] (N.J.S.); [email protected] (F.H.)
Published 12 April 2013, Science 340, 157 (2013)
DOI: 10.1126/science.1231828
This PDF file includes:
Table S1
Fig. S1
References
2
Table S1. Behaviors regulated by neuronal activity of vertebrate basal ganglia and insect central complex. Vertebrate Basal Ganglia Insect Central Complex Striatum, Globus Pallidus Protocerebral Bridge, Subthalamic nucleus, Fan-Shaped Body, Ellipsoid Body, Substantia nigra Lateral Accessory Lobe ___________________________________________________________________________________ Postural muscle tone (78) Coordinated locomotion (78) Coordinated locomotion (47) Goal-directed movement (79) Goal-directed movement (47) Saccadic eye movement (78)
Visual orientation and Visual orientation and space integration (80) space integration (25) Sleep (78) Sleep (39, 41, 82) Arousal (78) Arousal (39, 83) Attention (78) Attention (84) Courtship/sexual behavior (85) Sensorimotor learning (81) Place memory (86, 87) Habit learning (4, 81) Reward-seeking behavior (4, 80) Reward-seeking behavior (40, 43, 88) Emotional expression (78) ___________________________________________________________________________________
3
Fig. S1. Frontal autofluorescent section of the brain of the fruit fly, Drosophila melanogaster showing the mid-line position (box) of the central complex’s fan-shaped body. The 3-dimensional reconstruction (modified from ref. 47) illustrates the sequence of central complex synaptic neuropils and their spatial arrangements. Rostro-caudally these are: the protocerebral bridge (PB), the fan-shaped body (FB), the noduli (NO), the ellipsoid body (EB), and the lateral accessory complex (LX) comprising the lateral accessory lobe (LAL) and bulb (BU). In Drosophila, but not in other arthropods, the lateral margins of ellipsoid body meet at the midline to form an almost perfect torus.
1
References
1. M. Stephenson-Jones, E. Samuelsson, J. Ericsson, B. Robertson, S. Grillner, Evolutionary
conservation of the basal ganglia as a common vertebrate mechanism for action selection.
Curr. Biol. 21, 1081 (2011). doi:10.1016/j.cub.2011.05.001 Medline
2. S. Grillner, J. Hellgren, A. Ménard, K. Saitoh, M. A. Wikström, Mechanisms for selection of
basic motor programs—roles for the striatum and pallidum. Trends Neurosci. 28, 364
(2005). doi:10.1016/j.tins.2005.05.004 Medline
3. A. M. Graybiel, The basal ganglia. Curr. Biol. 10, R509 (2000). doi:10.1016/S0960-
9822(00)00593-5 Medline
4. P. Redgrave et al., Goal-directed and habitual control in the basal ganglia: Implications for
Parkinson’s disease. Nat. Rev. Neurosci. 11, 760 (2010). doi:10.1038/nrn2915 Medline
5. N. J. Strausfeld, Arthropod Brains: Evolution, Functional Elegance, and Historical
Significance (Harvard Univ. Press, Cambridge, MA, 2012).
6. K. Furukubo-Tokunaga, Z. N. Ludlow, F. Hirth, in Memory Mechanisms in Health and
Disease, K. P. Giese, Ed. (World Scientific, Singapore, 2012), pp. 269–306.
7. S. W. Wilson, J. L. Rubenstein, Induction and dorsoventral patterning of the telencephalon.
Neuron 28, 641 (2000). doi:10.1016/S0896-6273(00)00171-9 Medline
8. D. Carlin et al., Six3 cooperates with Hedgehog signaling to specify ventral telencephalon by
promoting early expression of Foxg1a and repressing Wnt signaling. Development 139,
2614 (2012). doi:10.1242/dev.076018 Medline
9. A. Simeone, E. Puelles, D. Acampora, The Otx family. Curr. Opin. Genet. Dev. 12, 409
(2002). doi:10.1016/S0959-437X(02)00318-0 Medline
10. M. P. Smidt, J. P. Burbach, How to make a mesodiencephalic dopaminergic neuron. Nat.
Rev. Neurosci. 8, 21 (2007). doi:10.1038/nrn2039 Medline
11. F. Hirth, On the origin and evolution of the tripartite brain. Brain Behav. Evol. 76, 3 (2010).
doi:10.1159/000320218 Medline
2
12. R. Urbach, G. M. Technau, Dorsoventral patterning of the brain: A comparative approach.
Adv. Exp. Med. Biol. 628, 42 (2008). doi:10.1007/978-0-387-78261-4_3 Medline
13. N. Posnien, N. D. Koniszewski, H. J. Hein, G. Bucher, Candidate gene screen in the red flour
beetle Tribolium reveals six3 as ancient regulator of anterior median head and central
complex development. PLoS Genet. 7, e1002416 (2011).
doi:10.1371/journal.pgen.1002416 Medline
14. F. Hirth et al., Developmental defects in brain segmentation caused by mutations of the
homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15, 769
(1995). doi:10.1016/0896-6273(95)90169-8 Medline
15. J. Blanco, R. Pandey, M. Wasser, G. Udolph, Orthodenticle is necessary for survival of a
cluster of clonally related dopaminergic neurons in the Drosophila larval and adult brain.
Neural Dev. 6, 34 (2011). doi:10.1186/1749-8104-6-34 Medline
16. P. Callaerts et al., Drosophila Pax-6/eyeless is essential for normal adult brain structure and
function. J. Neurobiol. 46, 73 (2001). doi:10.1002/1097-4695(20010205)46:2<73::AID-
NEU10>3.0.CO;2-N Medline
17. A. W. Flaherty, A. M. Graybiel, Input-output organization of the sensorimotor striatum in the
squirrel monkey. J. Neurosci. 14, 599 (1994). Medline
18. F. Eblen, A. M. Graybiel, Highly restricted origin of prefrontal cortical inputs to striosomes
in the macaque monkey. J. Neurosci. 15, 5999 (1995). Medline
19. A. M. Graybiel, T. Aosaki, A. W. Flaherty, M. Kimura, The basal ganglia and adaptive
motor control. Science 265, 1826 (1994). doi:10.1126/science.8091209 Medline
20. K.-I. Amemori, L. G. Gibb, A. M. Graybiel, Shifting responsibly: The importance of striatal
modularity to reinforcement learning in uncertain environments. Front. Hum. Neurosci.
5, 47 (2011). doi:10.3389/fnhum.2011.00047 Medline
21. U. Hanesch, K.-F. Fischbach, M. Heisenberg, Neuronal architecture of the central complex in
Drosophila melanogaster. Cell Tissue Res. 257, 343 (1989). doi:10.1007/BF00261838
22. K. Ito, T. Awasaki, Clonal unit architecture of the adult fly brain. Adv. Exp. Med. Biol. 628,
137 (2008). doi:10.1007/978-0-387-78261-4_9 Medline
3
23. Z. Herbert et al., Developmental expression of neuromodulators in the central complex of the
grasshopper Schistocerca gregaria. J. Morphol. 271, 1509 (2010).
doi:10.1002/jmor.10895 Medline
24. G. Boyan, L. Williams, Embryonic development of the insect central complex: Insights from
lineages in the grasshopper and Drosophila. Arthropod Struct. Dev. 40, 334 (2011).
doi:10.1016/j.asd.2011.02.005 Medline
25. U. Homberg, S. Heinze, K. Pfeiffer, M. Kinoshita, B. el Jundi, Central neural coding of sky
polarization in insects. Philos. Trans. R. Soc. London Ser. B 366, 680 (2011).
doi:10.1098/rstb.2010.0199 Medline
26. R. E. Ritzmann, A. L. Ridgel, A. J. Pollack, Multi-unit recording of antennal mechano-
sensitive units in the central complex of the cockroach, Blaberus discoidalis. J. Comp.
Physiol. A 194, 341 (2008). doi:10.1007/s00359-007-0310-2 Medline
27. P. Guo, R. E. Ritzmann, Neural activity in the central complex of the cockroach brain is
linked to turning behaviors. J. Exp. Biol. 216, 992 (2013). doi:10.1242/jeb.080473
Medline
28. H. Ghaffar, J. Larsen, G. Booth, R. Perkes, General morphology of the brain of the blind
cave beetle, Neaphaenops tellkampfii Erichson (Coleoptera: Carabidae). Int. J. Insect
Morphol. Embryol. 13, 357 (1984). doi:10.1016/0020-7322(84)90011-4
29. G. Liu et al., Distinct memory traces for two visual features in the Drosophila brain. Nature
439, 551 (2006). doi:10.1038/nature04381 Medline
30. J. Phillips-Portillo, The central complex of the flesh fly, Neobellieria bullata: Recordings and
morphologies of protocerebral inputs and small-field neurons. J. Comp. Neurol. 520,
3088 (2012). doi:10.1002/cne.23134 Medline
31. S. Kuntz, B. Poeck, M. B. Sokolowski, R. Strauss, The visual orientation memory of
Drosophila requires Foraging (PKG) upstream of Ignorant (RSK2) in ring neurons of the
central complex. Learn. Mem. 19, 337 (2012). doi:10.1101/lm.026369.112 Medline
32. U. Homberg, H. Vitzthum, M. Müller, U. Binkle, Immunocytochemistry of GABA in the
central complex of the locust Schistocerca gregaria: Identification of immunoreactive
4
neurons and colocalization with neuropeptides. J. Comp. Neurol. 409, 495 (1999).
doi:10.1002/(SICI)1096-9861(19990705)409:3<495::AID-CNE12>3.0.CO;2-F Medline
33. L. Kahsai, M. A. Carlsson, A. M. Winther, D. R. Nässel, Distribution of metabotropic
receptors of serotonin, dopamine, GABA, glutamate, and short neuropeptide F in the
central complex of Drosophila. Neuroscience 208, 11 (2012).
doi:10.1016/j.neuroscience.2012.02.007 Medline
34. L. Kahsai, A. M. Winther, Chemical neuroanatomy of the Drosophila central complex:
Distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol.
519, 290 (2011). doi:10.1002/cne.22520 Medline
35. J. P. Bolam, J. J. Hanley, P. A. Booth, M. D. Bevan, Synaptic organisation of the basal
ganglia. J. Anat. 196, 527 (2000). doi:10.1046/j.1469-7580.2000.19640527.x Medline
36. C. R. Gerfen, D. J. Surmeier, Modulation of striatal projection systems by dopamine. Annu.
Rev. Neurosci. 34, 441 (2011). doi:10.1146/annurev-neuro-061010-113641 Medline
37. Z. Mao, R. L. Davis, Eight different types of dopaminergic neurons innervate the Drosophila
mushroom body neuropil: Anatomical and physiological heterogeneity. Front. Neural
Circuits 3, 5 (2009). doi:10.3389/neuro.04.005.2009 Medline
38. K. E. White, D. M. Humphrey, F. Hirth, The dopaminergic system in the aging brain of
Drosophila. Front Neurosci 4, 205 (2010). doi:10.3389/fnins.2010.00205 Medline
39. T. Ueno et al., Identification of a dopamine pathway that regulates sleep and arousal in
Drosophila. Nat. Neurosci. 15, 1516 (2012). doi:10.1038/nn.3238 Medline
40. M. J. Krashes et al., A neural circuit mechanism integrating motivational state with memory
expression in Drosophila. Cell 139, 416 (2009). doi:10.1016/j.cell.2009.08.035 Medline
41. Q. Liu, S. Liu, L. Kodama, M. R. Driscoll, M. N. Wu, Two dopaminergic neurons signal to
the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 22, 2114
(2012). doi:10.1016/j.cub.2012.09.008 Medline
42. Y. C. Kim, H. G. Lee, C. S. Seong, K. A. Han, Expression of a D1 dopamine receptor
dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr.
Patterns 3, 237 (2003). doi:10.1016/S1567-133X(02)00098-4 Medline
5
43. E. C. Kong et al., A pair of dopamine neurons target the D1-like dopamine receptor DopR in
the central complex to promote ethanol-stimulated locomotion in Drosophila. PLoS ONE
5, e9954 (2010). doi:10.1371/journal.pone.0009954 Medline
44. T. J. Lewandowski, H. K. Lehman, S. C. Chamberlain, Immunoreactivity in Limulus: III.
Morphological and biochemical studies of FMRFamide-like immunoreactivity and
colocalized substance P-like immunoreactivity in the brain and lateral eye. J. Comp.
Neurol. 288, 136 (1989). doi:10.1002/cne.902880111 Medline
45. K. Langworthy, S. Helluy, J. Benton, B. Beltz, Amines and peptides in the brain of the
American lobster: Immunocytochemical localization patterns and implications for brain
function. Cell Tissue Res. 288, 191 (1997). doi:10.1007/s004410050806 Medline
46. H. Vitzthum, U. Homberg, Immunocytochemical demonstration of locustatachykinin-related
peptides in the central complex of the locust brain. J. Comp. Neurol. 390, 455 (1998).
doi:10.1002/(SICI)1096-9861(19980126)390:4<455::AID-CNE1>3.0.CO;2-# Medline
47. R. Strauss, The central complex and the genetic dissection of locomotor behaviour. Curr.
Opin. Neurobiol. 12, 633 (2002). doi:10.1016/S0959-4388(02)00385-9 Medline
48. E. Tupala, J. Tiihonen, Dopamine and alcoholism: Neurobiological basis of ethanol abuse.
Prog. Neuropsychopharmacol. Biol. Psychiatry 28, 1221 (2004).
doi:10.1016/j.pnpbp.2004.06.022 Medline
49. T. Riemensperger et al., Behavioral consequences of dopamine deficiency in the Drosophila
central nervous system. Proc. Natl. Acad. Sci. U.S.A. 108, 834 (2011).
doi:10.1073/pnas.1010930108 Medline
50. F. Hirth, Drosophila melanogaster in the study of human neurodegeneration. CNS Neurol.
Disord. Drug Targets 9, 504 (2010). doi:10.2174/187152710791556104 Medline
51. D. M. Humphrey et al., Alternative oxidase rescues mitochondria-mediated dopaminergic
cell loss in Drosophila. Hum. Mol. Genet. 21, 2698 (2012). doi:10.1093/hmg/dds096
Medline
52. G. Schumann et al., Genome-wide association and genetic functional studies identify autism
susceptibility candidate 2 gene (AUTS2) in the regulation of alcohol consumption. Proc.
Natl. Acad. Sci. U.S.A. 108, 7119 (2011). doi:10.1073/pnas.1017288108 Medline
6
53. R. G. Northcutt, Evolution of centralized nervous systems: Two schools of evolutionary
thought. Proc. Natl. Acad. Sci. U.S.A. 109 (suppl. 1), 10626 (2012).
doi:10.1073/pnas.1201889109 Medline
54. F. Christodoulou et al., Ancient animal microRNAs and the evolution of tissue identity.
Nature 463, 1084 (2010). doi:10.1038/nature08744 Medline
55. J. Mallatt, C. W. Craig, M. J. Yoder, Nearly complete rRNA genes from 371 Animalia:
Updated structure-based alignment and detailed phylogenetic analysis. Mol. Phylogenet.
Evol. 64, 603 (2012). doi:10.1016/j.ympev.2012.05.016 Medline
56. P. R. Steinmetz et al., Independent evolution of striated muscles in cnidarians and bilaterians.
Nature 487, 231 (2012). doi:10.1038/nature11180 Medline
57. X. Ma, X. Hou, G. D. Edgecombe, N. J. Strausfeld, Complex brain and optic lobes in an
early Cambrian arthropod. Nature 490, 258 (2012). doi:10.1038/nature11495 Medline
58. B. K. Hall, Descent with modification: The unity underlying homology and homoplasy as
seen through an analysis of development and evolution. Biol. Rev. Camb. Philos. Soc. 78,
409 (2003). doi:10.1017/S1464793102006097 Medline
59. D. M. Raup, A. Seilacher, Fossil foraging behavior: Computer simulation. Science 166, 994
(1969). doi:10.1126/science.166.3908.994 Medline
60. L. A. Buatois, M. G. Mángano, An Early Cambrian shallow-marine ichnofauna from the
Puncoviscana Formation of Northwest Argentina: The interplay between sophisticated
feeding behaviors, matgrounds and sea-level changes. J. Paleontol. 86, 7 (2012).
doi:10.1666/11-001.1
61. R. Tomer, A. S. Denes, K. Tessmar-Raible, D. Arendt, Profiling by image registration
reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142,
800 (2010). doi:10.1016/j.cell.2010.07.043 Medline
62. J. L. Rubenstein, K. Shimamura, S. Martinez, L. Puelles, Regionalization of the
prosencephalic neural plate. Annu. Rev. Neurosci. 21, 445 (1998).
doi:10.1146/annurev.neuro.21.1.445 Medline
7
63. W. Ye, K. Shimamura, J. L. Rubenstein, M. A. Hynes, A. Rosenthal, FGF and Shh signals
control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755
(1998). doi:10.1016/S0092-8674(00)81437-3 Medline
64. L. Sussel, O. Marin, S. Kimura, J. L. Rubenstein, Loss of Nkx2.1 homeobox gene function
results in a ventral to dorsal molecular respecification within the basal telencephalon:
Evidence for a transformation of the pallidum into the striatum. Development 126, 3359
(1999). Medline
65. T. Mueller, M. F. Wullimann, S. Guo, Early teleostean basal ganglia development visualized
by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression. J. Comp.
Neurol. 507, 1245 (2008). doi:10.1002/cne.21604 Medline
66. H. Toresson, K. A. Campbell, A role for Gsh1 in the developing striatum and olfactory bulb
of Gsh2 mutant mice. Development 128, 4769 (2001). Medline
67. L. Muzio et al., Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey)
double-mutant mice. Nat. Neurosci. 5, 737 (2002). Medline
68. A. Abeliovich, R. Hammond, Midbrain dopamine neuron differentiation: Factors and fates.
Dev. Biol. 304, 447 (2007). doi:10.1016/j.ydbio.2007.01.032 Medline
69. S. T. Philips, R. L. Albin, D. M. Martin, Exp. Neurol. 192, 320 (2005).
70. D. M. Martin et al., PITX2 is required for normal development of neurons in the mouse
subthalamic nucleus and midbrain. Dev. Biol. 267, 93 (2004).
doi:10.1016/j.ydbio.2003.10.035 Medline
71. F. Hirth, H. Reichert, in Evolution of Nervous Systems, Vol. I, T. H. Bullock et al., Eds.
(Elsevier, London, 2005), pp. 55–72.
72. B. Poeck, T. Triphan, K. Neuser, R. Strauss, Locomotor control by the central complex in
Drosophila—An analysis of the tay bridge mutant. Dev. Neurobiol. 68, 1046 (2008).
doi:10.1002/dneu.20643 Medline
73. M. Desban, C. Gauchy, M. L. Kemel, M. J. Besson, J. Glowinski, Three-dimensional
organization of the striosomal compartment and patchy distribution of striatonigral
8
projections in the matrix of the cat caudate nucleus. Neuroscience 29, 551 (1989).
doi:10.1016/0306-4522(89)90130-9 Medline
74. K. Ito et al., The organization of extrinsic neurons and their implications in the functional
roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52
(1998). Medline
75. M. Iwano et al., Neurons associated with the flip-flop activity in the lateral accessory lobe
and ventral protocerebrum of the silkworm moth brain. J. Comp. Neurol. 518, 366
(2010). doi:10.1002/cne.22224 Medline
76. M. W. Shiflett, B. W. Balleine, Molecular substrates of action control in cortico-striatal
circuits. Prog. Neurobiol. 95, 1 (2011). doi:10.1016/j.pneurobio.2011.05.007 Medline
77. W. Gronenberg, N. J. Strausfeld, Premotor descending neurons responding selectively to
local visual stimuli in flies. J. Comp. Neurol. 316, 87 (1992). doi:10.1002/cne.903160108
Medline
78. K. Takakusaki, K. Saitoh, H. Harada, M. Kashiwayanagi, Role of basal ganglia-brainstem
pathways in the control of motor behaviors. Neurosci. Res. 50, 137 (2004).
doi:10.1016/j.neures.2004.06.015 Medline
79. K. P. Bhatia, C. D. Marsden, The behavioural and motor consequences of focal lesions of the
basal ganglia in man. Brain 117, 859 (1994). doi:10.1093/brain/117.4.859 Medline
80. M. D. Humphries, T. J. Prescott, The ventral basal ganglia, a selection mechanism at the
crossroads of space, strategy, and reward. Prog. Neurobiol. 90, 385 (2010).
doi:10.1016/j.pneurobio.2009.11.003 Medline
81. A. M. Graybiel, Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359
(2008). doi:10.1146/annurev.neuro.29.051605.112851 Medline
82. J. M. Donlea, M. S. Thimgan, Y. Suzuki, L. Gottschalk, P. J. Shaw, Inducing sleep by remote
control facilitates memory consolidation in Drosophila. Science 332, 1571 (2011).
doi:10.1126/science.1202249 Medline
9
83. T. Lebestky et al., Two different forms of arousal in Drosophila are oppositely regulated by
the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64, 522
(2009). doi:10.1016/j.neuron.2009.09.031 Medline
84. B. Van Swinderen, R. Andretic, Dopamine in Drosophila: Setting arousal thresholds in a
miniature brain. Proc. Biol. Sci. 278, 906 (2011). doi:10.1098/rspb.2010.2564 Medline
85. T. Sakai, T. Kitamoto, Differential roles of two major brain structures, mushroom bodies and
central complex, for Drosophila male courtship behavior. J. Neurobiol. 66, 821 (2006).
doi:10.1002/neu.20262 Medline
86. K. Neuser, T. Triphan, M. Mronz, B. Poeck, R. Strauss, Analysis of a spatial orientation
memory in Drosophila. Nature 453, 1244 (2008). doi:10.1038/nature07003 Medline
87. T. A. Ofstad, C. S. Zuker, M. B. Reiser, Visual place learning in Drosophila melanogaster.
Nature 474, 204 (2011). doi:10.1038/nature10131 Medline
88. A. Claridge-Chang et al., Writing memories with light-addressable reinforcement circuitry.
Cell 139, 405 (2009). doi:10.1016/j.cell.2009.08.034 Medline