Evolution of cortical inhibitory GABAergic neurons

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Changes in cortical interneuron migration contribute to the evolution of the neocortex http://www.pnas.org/content/108/19/8015.short

Evolutionary developmental basis in the
adaptation of pallial GABAergic interneurons to
mammalian layered neocortex!
Daisuke H. Tanaka, Ryo Oiwa1, Erika Sasaki1 and Kazunori Nakajima!
Department of Anatomy, Keio Univ.Sch. of Med.!
1CIEA!

Origin and migratory pathways for cortical neurons in mice!
Dorsal!
Medial!
Marginal zone (MZ)!
Cortical plate (CP)!
Intermediate zone (IZ)!
Ventricular zone (VZ)!
Subventricular zone (SVZ)!
Projection neurons!
Ventricle!
Neocortex!
Pia!
Subplate (SP)!

Origin and migratory pathways for cortical neurons in mice!
Medial ganglionic!
eminence (MGE)!
Pia!
Ventricle!
1!
2!
“ 2-step migration ”!
Marginal zone (MZ)!
Cortical plate (CP)!
Intermediate zone (IZ)!
Ventricular zone (VZ)!
Subventricular zone (SVZ)!
Subplate (SP)!
Interneurons!
GABAergic!
Neocortex!

2-step migration is speciﬁc to mammals!
mammals!
sauropsids!
(monkey, mouse)!
(turtle, chicken)!
2-step migration!
mammal
interneurons!
sauropsid !
interneurons!
SVZ!
SVZ!
?!

Non-cell-autonomous Hypothesis !
mammal-speciﬁc 2-step migration is caused by mammal-speciﬁc
cortical environment!
mammals!
sauropsids!
(monkey, mouse)!
(turtle, chicken)!
SVZ!
2-step migration!
sauropsid !
interneuron!
SVZ!

Interspecies transplantation!

Chicken MGE cells migrated tangentially toward the mouse cortex!
Chicken MGE! Chicken DVR!
MouseMGE!DAPI!
E13.5:E15.5!
neocortex!
MGE!

Chicken cells migrated in the SVZ, but failed to leave there!

Sauropsid cells migrated in the SVZ, but failed to leave there!
Chicken!
Turtle!
Marmoset!

Sauropsid cells migrated in the SVZ, but failed to leave there!
MZ!
CP!
IZ!
VZ!
SVZ!
Pia!
Ventricle!
1!
2!
Mouse!
Chicken!
Marmoset!
Turtle!
1!
2!

Non-cell-autonomous Hypothesis !
mammal-speciﬁc 2-step migration is due to mammal-speciﬁc
cortical environment!
mammals!
sauropsids!
(monkey, mouse)!
(turtle, chicken)!
SVZ!
2-step migration!
sauropsid !
interneuron!
SVZ!
Non-cell-autonomous!
Cell-autonomous!

mammals!
sauropsids!
(monkey, mouse)!
(turtle, chicken)!
2-step migration!
1st!
2nd!
Pre-adaptation to mammal SVZ cells !
may underlie interneuron-migration evolution!
MGE-cell competency!
1st step!
2nd step!
SVZ!
attract MGE cells!
required for 1st step!
(Tiveron et al., 2006; Sessa et al.,2010)!
Responsiveness to SVZ!
=!

Acknowledgement!
Yasunori Murakami!
Ehime Univ.!
Yan Zhu!
Osaka Univ.!
Fujio Murakami!
Shinji Sasaki!
Keio Univ. Sch. of Med.!
Takehiko Sunabori!
Michisuke Yuzaki!
Hiroshi Nagashima!
RIKEN CDB!
Hideyuki Okano!
Kazuhisa Kohda!
Shuta Tomisato!
Masaru Okabe!

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1. Evolutionary developmental basis in the adaptation of pallial GABAergic interneurons to mammalian layered neocortex! Daisuke H. Tanaka, Ryo Oiwa1, Erika Sasaki1 and Kazunori Nakajima! Department of Anatomy, Keio Univ.Sch. of Med.! 1CIEA!

2. Origin and migratory pathways for cortical neurons in mice! Dorsal! Medial! Marginal zone (MZ)! Cortical plate (CP)! Intermediate zone (IZ)! Ventricular zone (VZ)! Subventricular zone (SVZ)! Projection neurons! Ventricle! Neocortex! Pia! Subplate (SP)!

3. Origin and migratory pathways for cortical neurons in mice! Medial ganglionic! eminence (MGE)! Pia! Ventricle! 1! 2! “ 2-step migration ”! Marginal zone (MZ)! Cortical plate (CP)! Intermediate zone (IZ)! Ventricular zone (VZ)! Subventricular zone (SVZ)! Subplate (SP)! Interneurons! GABAergic! Neocortex!

4. 2-step migration is speciﬁc to mammals! mammals! sauropsids! (monkey, mouse)! (turtle, chicken)! 2-step migration! mammal interneurons! sauropsid ! interneurons! SVZ! SVZ! ?!

5. Non-cell-autonomous Hypothesis ! mammal-speciﬁc 2-step migration is caused by mammal-speciﬁc cortical environment! mammals! sauropsids! (monkey, mouse)! (turtle, chicken)! SVZ! 2-step migration! sauropsid ! interneuron! SVZ!

6. Interspecies transplantation!

7. Chicken MGE cells migrated tangentially toward the mouse cortex! Chicken MGE! Chicken DVR! MouseMGE!DAPI! E13.5:E15.5! neocortex! MGE!

8. Chicken cells migrated in the SVZ, but failed to leave there!

9. Sauropsid cells migrated in the SVZ, but failed to leave there! Chicken! Turtle! Marmoset!

10. Sauropsid cells migrated in the SVZ, but failed to leave there! MZ! CP! IZ! VZ! SVZ! Pia! Ventricle! 1! 2! Mouse! Chicken! Marmoset! Turtle! 1! 2!

11. Non-cell-autonomous Hypothesis ! mammal-speciﬁc 2-step migration is due to mammal-speciﬁc cortical environment! mammals! sauropsids! (monkey, mouse)! (turtle, chicken)! SVZ! 2-step migration! sauropsid ! interneuron! SVZ! Non-cell-autonomous! Cell-autonomous!

12. mammals! sauropsids! (monkey, mouse)! (turtle, chicken)! 2-step migration! 1st! 2nd! Pre-adaptation to mammal SVZ cells ! may underlie interneuron-migration evolution! MGE-cell competency! 1st step! 2nd step! SVZ! attract MGE cells! required for 1st step! (Tiveron et al., 2006; Sessa et al.,2010)! Responsiveness to SVZ! =!

13. Acknowledgement! Yasunori Murakami! Ehime Univ.! Yan Zhu! Osaka Univ.! Fujio Murakami! Shinji Sasaki! Keio Univ. Sch. of Med.! Takehiko Sunabori! Michisuke Yuzaki! Hiroshi Nagashima! RIKEN CDB! Hideyuki Okano! Kazuhisa Kohda! Shuta Tomisato! Masaru Okabe!