Developmental changes in dendritic shape and synapse location tune single-neuron computations to changing behavioral functions

Journal of Neurophysiology

Volumn 102, Issue 1, 2009, Pages 41-58

  Meseke, Maurice ^a   Evers, Jan Felix ^b   Duch, Carsten ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; SYNAPSIN I;

ARTICLE; BEHAVIOR; CONFOCAL LASER MICROSCOPY; DENDRITE; DEVELOPMENTAL STAGE; GABAERGIC TRANSMISSION; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; MORPHOMETRICS; MOTONEURON; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; SYNAPTOGENESIS;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; COMPUTER SIMULATION; DENDRITES; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; GANGLIA, INVERTEBRATE; MANDUCA; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, CONFOCAL; MODELS, NEUROLOGICAL; MOTOR NEURONS; SYNAPSES; SYNAPSINS;

EID: 67649625146     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90899.2008     Document Type: Article

References (47)

1. Andrasfalvy BK, Magee JC. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21: 9151-9159, 2001. (Pubitemid 33096858)
2. Bell RA, Joachim FA. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69: 365-373, 1976.
3. Burrows M. The Neurobiology of an Insect Brain. Oxford, UK: Oxford Univ. Press, 1996.
4. Chklovskii DB, Schikorski T, Stevens CF. Wiring optimization in cortical circuits. Neuron 34: 341-347, 2000. (Pubitemid 34465493)
5. Consoulas C, Duch C, Bayline RJ, Levine RB. Behavioral transformations during metamorphosis: remodeling of neural and motor systems. Brain Res Bull 15: 571-583, 2000. (Pubitemid 32114310)
6. Craig AM, Banker G. Neuronal polarity. Annu Rev Neurosci 17: 267-310, 1994. (Pubitemid 24117032)
7. Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, Svoboda K, Huang ZJ. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of thalamic inputs. Nat Neurosci 7: 1184-1186, 2004. (Pubitemid 39426235)
8. Duch C, Bayline RJ, Levine RB. Postembryonic development of the dorsal longitudinal flight muscle and its innervation in Manduca sexta. J Comp Neurol 422: 1-17, 2000. (Pubitemid 30346561)
9. Duch C, Levine RB. Changes in calcium signaling during postembryonic dendritic growth in Manduca sexta. J Neurophysiol 87: 1415-1425, 2002. (Pubitemid 34670809)
10. Duch C, Levine RB. Remodeling of membrane properties and dendritic architecture accompany the postembryonic conversion of a "slow" into a "fast" motoneuron. J Neurosci 20: 6950-6961, 2000.
11. Duch C, Mentel T. Activity affects dendritic shape and synapse elimination during steroid controlled dendritic retraction in Manduca sexta. J Neurosci 24: 9826-9837, 2004. (Pubitemid 39463563)
12. Evers JF, Muench D, Duch C. Developmental relocation of presynaptic terminals along distinct types of dendritic filopodia. Dev Biol 297: 214-227, 2006. (Pubitemid 44301104)
13. Evers JF, Schmitt S, Scholz M, Duch C. New frontiers in functional neuroanatomy: precise automatic reconstruction from confocal image stacks. J Neurophysiol 93: 2331-2342, 2005.
14. Gabbiani F, Krapp HG, Koch C, Laurent G. Multiplicative computation in a visual neuron sensitive to looming. Nature 420: 320-324, 2002. (Pubitemid 35398187)
15. Hohensee S, Bleiss W, Duch C. Correlative electron and confocal microscopy assessment of synapse localization in the central nervous system of an insect. J Neurosci Methods 168: 64-70, 2008.
16. Hooper SC, Guschlbauer C, von Uckerman G, Bueschges A. Different motor neuron spike patterns produce contractions with very similar rises in graded slow muscles. J Neurophysiol 97: 1428-1444, 2007. (Pubitemid 46239519)
17. Horton AC, Ehlers MD. Neuronal polarity and trafficking. Neuron 40: 277-295, 2003. (Pubitemid 37247602)
18. Huang EJ, Reichardt LF. TRK receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642, 2003. (Pubitemid 36930455)
19. Kapfer C, Seidle AH, Schweizer H, Grothe B. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci 5: 247-253, 2002. (Pubitemid 34171138)
20. Kinnamon SC, Klaassen LW, Kammer AE, Claassen D. Octopamine and chlordimeform enhance sensory responsiveness and production of the flight motor pattern in developing and adult moths. J Neurobiol 15: 283-293, 1984. (Pubitemid 14056031)
21. Koch C. Computation and the single neuron. Nature 385: 207-210, 1997. (Pubitemid 27043708)
22. Koch C, Segev I. The role of single neurons in information processing. Nat Neurosci 3: 1171-1177, 2000.
23. Libersat F, Duch C. Morphometric analysis of dendritic remodeling in an identified motoneuron during postembryonic development. J Comp Neurol 450: 153-166, 2002. (Pubitemid 34803913)
24. + channel in hippocampal neurons. Neuron 25: 385-397, 2000.
25. London M, Haeusser M. Dendritic computation. Annu Rev Neurosci 28: 503-532, 2005. (Pubitemid 41098913)
26. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1988.
27. Magee JC, Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal neurons. Nat Neurosci 3: 895-903, 2000. (Pubitemid 30677176)
28. Mentel T, Duch C. Stage-specific activity patterns affect motoneuron axonal retraction and outgrowth during the metamorphosis of Manduca sexta. Eur J Neurosci 17: 945-962, 2003. (Pubitemid 36411592)
29. Meseke M, Evers JF, Duch C. PTX-induced hyperexcitability affects dendritic shape and GABAergic synapse density but not synapse distribution during Manduca postembryonic motoneuron development. J Comp Physiol A Epub ahead of print, 2009.
30. Morris LG, Hooper SL. Muscle response to changing neuronal input in the lobster (Panulirus interruptus) stomatogastric system: slow muscle properties can transform rhythmic input into tonic output. J Neurosci 18: 3433-3442, 1998. (Pubitemid 28186034)
31. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsaki G, Siegelbaum SA, Kandel ER, Morozov A. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119: 719-732, 2004. (Pubitemid 39535758)
32. Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293: 1159-1163, 2001. (Pubitemid 32758100)
33. Reinecke JP, Buckner JS, Grugel SR. Life-cycle of laboratory-reared tobacco hornworms, Manduca sexta - study of development and behavior, using time-lapse cinematography. Biol Bull 158: 129-140, 1980.
34. Schmitt S, Evers JF, Scholz M, Duch C, Obermayer K. New methods for the computer assisted 3D reconstruction of neurons from confocal image stacks. Neuroimage 23: 1283-1298, 2004. (Pubitemid 40260352)
35. Sholl DA. Dendritic organization in the neurons of the visual cortex and motor cortices of the cat. J Anat 87: 387-406, 1953.
36. Single S, Borst A. Dendritic integration and its role in computing image velocity. Science 281: 1848-1850, 1998. (Pubitemid 28450504)
37. Somogyi P, Tamas G, Lujan R, Buhl EH. Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26: 1113-1135, 1998. (Pubitemid 28318069)
38. Stepanyants A, Chklovskii DB. Neurogeometry and potential synaptic connectivity. Trends Neurosci 28: 387-394, 2005. (Pubitemid 40853862)
39. Stepanyants A, Hof PR, Chklovskii DB. Geometry and structural plasticity of synaptic connectivity. Neuron 34: 275-288, 2002. (Pubitemid 34442570)
40. Stricker C, Field AC, Redman SJ. Changes in quantal parameters of EPSCs in rat CA1 neurons in vitro after the induction of long-term potentiation. J Physiol 490: 443-454, 1996. (Pubitemid 26032958)
41. Tissot M, Stocker RF. Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog Neurobiol 62: 89-111, 2000. (Pubitemid 30252018)
42. Tolbert LP, Matsumoto SG, Hildebrandt JG. Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3: 1158-1175, 1983.
43. Tu MS, Daniel TE. Submaximal power output from the dorsolongitudinal flight muscles of the hawkmoth Manduca sexta. J Exp Biol 207: 4651-4662, 2004. (Pubitemid 40178065)
44. Watson AHD, Burrows M. Immunocytochemical and pharmacological evidence for GABAergic spiking local interneurons in the locust. J Neurosci 7: 1741-1751, 1987. (Pubitemid 17119796)
45. Watson AHD, Laurent G. GABA-like immunoreactivity in a population of locust intersegmental interneurones and their inputs. J Comp Neurol 302: 761-767, 1990.
46. Weeks JC. Thinking globally, acting locally: steroid hormone regulation of the dendritic architecture, synaptic connectivity and death of an individual neuron. Prog Neurobiol 70: 421-442, 2003. (Pubitemid 37159282)
47. Wildman M, Ott SR, Burrows M. GABA-like immunoreactivity in nonspiking interneurons of the locust metathoracic ganglion. J Exp Biol 205: 3651-3659, 2002. (Pubitemid 36010752)