 |
Previous Article | Next Article 
Journal of Neuroscience, Vol 14, 2161-2177, Copyright © 1994 by Society for Neuroscience
Dynamic behaviors of growth cones extending in the corpus callosum of living cortical brain slices observed with video microscopy
MC Halloran and K Kalil
Neuroscience Training Program, University of Wisconsin-Madison 53706.
During development, axons of the mammalian corpus callosum must navigate
across the midline to establish connections with corresponding targets in
the contralateral cerebral cortex. To gain insight into how growth cones of
callosal axons respond to putative guidance cues along this CNS pathway, we
have used time-lapse video microscopy to observe dynamic behaviors of
individual callosal growth cones extending in living brain slices from
neonatal hamster sensorimotor cortex. Crystals of the lipophilic dye
1,1'-dioctadecyl-3,3,3',3'- tetramethylindocarbocyanine perchlorate (Dil)
were inserted into the cortex in vivo to label small populations of
callosal axons and their growth cones. Subsequently, 400 microns brain
slices that included the injection site, the corpus callosum, and the
target cortex were placed in culture and viewed under low-light-level
conditions with a silicon- intensified target (SIT) camera. Time-lapse
video observations revealed striking differences in growth cone behaviors
in different regions of the callosal pathway. In the tract, which is
defined as the region of the callosal pathway from the injection site to
the corresponding target cortex, growth cones advanced rapidly, displaying
continual lamellipodial shape changes and filopodial exploration. Forward
advance was sometimes interrupted by brief pauses or retraction. Growth
cones in the target cortex had almost uniform compact shapes that were
consistently smaller than those in the tract. In cortex, axons adhered to
straight radial trajectories and their growth cones extended at only half
the speed of those in the tract. Growth cones in subtarget regions of the
callosum beneath cortical targets displayed complex behaviors characterized
by long pauses, extension of transitory branches, and repeated cycles of
collapse, withdrawal, and resurgence. Video observations suggested that
extension of axons into cortical targets could occur by interstitial
branching from callosal axons rather than by turning behaviors of the
primary growth cones. These results suggest the existence of guidance cues
distinct for each of these callosal regions that elicit characteristic
growth cone behaviors.
This article has been cited by other articles:

|
 |

|
 |
 
M. J. Galazo, V. Martinez-Cerdeno, C. Porrero, and F. Clasca
Embryonic and Postnatal Development of the Layer I-Directed ("Matrix") Thalamocortical System in the Rat
Cereb Cortex,
February 1, 2008;
18(2):
344 - 363.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. I. Hutchins and K. Kalil
Differential Outgrowth of Axons and their Branches Is Regulated by Localized Calcium Transients
J. Neurosci.,
January 2, 2008;
28(1):
143 - 153.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Lovell and L. L. Moroz
The largest growth cones in the animal kingdom: an illustrated guide to the dynamics of Aplysia neuronal growth in cell culture
Integr. Comp. Biol.,
December 1, 2006;
46(6):
847 - 870.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. E. Miller and M. P. Sheetz
Direct evidence for coherent low velocity axonal transport of mitochondria
J. Cell Biol.,
May 8, 2006;
173(3):
373 - 381.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Tang and K. Kalil
Netrin-1 Induces Axon Branching in Developing Cortical Neurons by Frequency-Dependent Calcium Signaling Pathways
J. Neurosci.,
July 13, 2005;
25(28):
6702 - 6715.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. W. Dent, A. M. Barnes, F. Tang, and K. Kalil
Netrin-1 and Semaphorin 3A Promote or Inhibit Cortical Axon Branching, Respectively, by Reorganization of the Cytoskeleton
J. Neurosci.,
March 24, 2004;
24(12):
3002 - 3012.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Tabata and K. Nakajima
Multipolar Migration: The Third Mode of Radial Neuronal Migration in the Developing Cerebral Cortex
J. Neurosci.,
November 5, 2003;
23(31):
9996 - 10001.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Raine, T. Lencz, K. Taylor, J. B. Hellige, S. Bihrle, L. Lacasse, M. Lee, S. Ishikawa, and P. Colletti
Corpus Callosum Abnormalities in Psychopathic Antisocial Individuals
Arch Gen Psychiatry,
November 1, 2003;
60(11):
1134 - 1142.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. W. Dent, F. Tang, and K. Kalil
Axon Guidance by Growth Cones and Branches: Common Cytoskeletal and Signaling Mechanisms
Neuroscientist,
October 1, 2003;
9(5):
343 - 353.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Tang, E. W. Dent, and K. Kalil
Spontaneous Calcium Transients in Developing Cortical Neurons Regulate Axon Outgrowth
J. Neurosci.,
February 1, 2003;
23(3):
927 - 936.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. W. Dent and K. Kalil
Axon Branching Requires Interactions between Dynamic Microtubules and Actin Filaments
J. Neurosci.,
December 15, 2001;
21(24):
9757 - 9769.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Teng, Y. Takei, A. Harada, T. Nakata, J. Chen, and N. Hirokawa
Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization
J. Cell Biol.,
October 1, 2001;
155(1):
65 - 76.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. T. N. Ba-Charvet, K. Brose, L. Ma, K. H. Wang, V. Marillat, C. Sotelo, M. Tessier-Lavigne, and A. Chedotal
Diversity and Specificity of Actions of Slit2 Proteolytic Fragments in Axon Guidance
J. Neurosci.,
June 15, 2001;
21(12):
4281 - 4289.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Szebenyi, E. W. Dent, J. L. Callaway, C. Seys, H. Lueth, and K. Kalil
Fibroblast Growth Factor-2 Promotes Axon Branching of Cortical Neurons by Influencing Morphology and Behavior of the Primary Growth Cone
J. Neurosci.,
June 1, 2001;
21(11):
3932 - 3941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Moses, E. Courchesne, J. Stiles, D. Trauner, B. Egaas, and E. Edwards
Regional Size Reduction in the Human Corpus Callosum Following Pre- and Perinatal Brain Injury
Cereb Cortex,
December 1, 2000;
10(12):
1200 - 1210.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Skaliora, R. Adams, and C. Blakemore
Morphology and Growth Patterns of Developing Thalamocortical Axons
J. Neurosci.,
May 15, 2000;
20(10):
3650 - 3662.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J. Diefenbach, P. B. Guthrie, and S. B. Kater
Stimulus History Alters Behavioral Responses of Neuronal Growth Cones
J. Neurosci.,
February 15, 2000;
20(4):
1484 - 1494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. W. Dent, J. L. Callaway, G. Szebenyi, P. W. Baas, and K. Kalil
Reorganization and Movement of Microtubules in Axonal Growth Cones and Developing Interstitial Branches
J. Neurosci.,
October 15, 1999;
19(20):
8894 - 8908.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. A. Davies, D. R. Goucher, C. Doller, and J. Silver
Robust Regeneration of Adult Sensory Axons in Degenerating White Matter of the Adult Rat Spinal Cord
J. Neurosci.,
July 15, 1999;
19(14):
5810 - 5822.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Knobel, E. Jorgensen, and M. Bastiani
Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans
Development,
January 10, 1999;
126(20):
4489 - 4498.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
V Castellani and J Bolz
Opposing roles for neurotrophin-3 in targeting and collateral formation of distinct sets of developing cortical neurons
Development,
January 8, 1999;
126(15):
3335 - 3345.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Ferhat, C. Cook, M. Chauviere, M. Harper, M. Kress, G. E. Lyons, and P. W. Baas
Expression of the Mitotic Motor Protein Eg5 in Postmitotic Neurons: Implications for Neuronal Development
J. Neurosci.,
October 1, 1998;
18(19):
7822 - 7835.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Szebenyi, J. L. Callaway, E. W. Dent, and K. Kalil
Interstitial Branches Develop from Active Regions of the Axon Demarcated by the Primary Growth Cone during Pausing Behaviors
J. Neurosci.,
October 1, 1998;
18(19):
7930 - 7940.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Gallo and P. C. Letourneau
Localized Sources of Neurotrophins Initiate Axon Collateral Sprouting
J. Neurosci.,
July 15, 1998;
18(14):
5403 - 5414.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P Lamoureux, R. Buxbaum, and S. Heidemann
Axonal outgrowth of cultured neurons is not limited by growth cone competition
J. Cell Sci.,
January 11, 1998;
111(21):
3245 - 3252.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Yamamoto, S. Higashi, and K. Toyama
Stop and Branch Behaviors of Geniculocortical Axons: A Time-Lapse Study in Organotypic Cocultures
J. Neurosci.,
May 15, 1997;
17(10):
3653 - 3663.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Wang and E. R. Macagno
The Establishment of Peripheral Sensory Arbors in the Leech: In Vivo Time-Lapse Studies Reveal a Highly Dynamic Process
J. Neurosci.,
April 1, 1997;
17(7):
2408 - 2419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Mason and L.-C. Wang
Growth Cone Form Is Behavior-Specific and, Consequently, Position-Specific along the Retinal Axon Pathway
J. Neurosci.,
February 1, 1997;
17(3):
1086 - 1100.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Henke-Fahle, F. Mann, M. Gotz, K. Wild, and J. Bolz
Dual Action of a Carbohydrate Epitope on Afferent and Efferent Axons in Cortical Development
J. Neurosci.,
July 1, 1996;
16(13):
4195 - 4206.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Dailey and S. J Smith
The Dynamics of Dendritic Structure in Developing Hippocampal Slices
J. Neurosci.,
May 1, 1996;
16(9):
2983 - 2994.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|