Development of tectal connectivity across metamorphosis in the bullfrog (Rana catesbeiana).
In the bullfrog (Rana catesbeiana), the process of metamorphosis culminates in the appearance of new visual and visuomotor behaviors reflective of the emergence of binocular vision and visually-guided prey capture behaviors as the animal transitions to life on land. Using several different neuroanatomical tracers, we examined the substrates that may underlie these behavioral changes by tracing the afferent and efferent connectivity of the midbrain optic tectum across metamorphic development. Intratectal, tectotoral, tectotegmental, tectobulbar, and tecto-thalamic tracts exhibit similar trajectories of neurobiotin fiber label across the developmental span from early larval tadpoles to adults. Developmental variability was apparent primarily in intensity and distribution of cell and puncta label in target nuclei. Combined injections of cholera toxin subunit β and Phaseolus vulgaris leucoagglutinin consistently label cell bodies, puncta, or fiber segments bilaterally in midbrain targets including the pretectal gray, laminar nucleus of the torus semicircularis, and the nucleus of the medial longitudinal fasciculus. Developmentally stable label was observed bilaterally in medullary targets including the medial vestibular nucleus, lateral vestibular nucleus, and reticular gray, and in forebrain targets including the posterior and ventromedial nuclei of the thalamus. The nucleus isthmi, cerebellum, lateral line nuclei, medial septum, ventral striatum, and medial pallium show more developmentally variable patterns of connectivity. Our results suggest that even during larval development, the optic tectum contains substrates for integration of visual with auditory, vestibular, and somatosensory cues, as well as for guidance of motivated behaviors.
Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, RI, USA.
Seth S
SS
Horowitz
Andrea Megela
AM
Simmons
D000818:Animals; D007814:Larva / Q000033:anatomy & histology / Q000254:growth & development; D008675:Metamorphosis, Biological / Q000502:physiology; D056347:Neuroanatomical Tract-Tracing Techniques; D009949:Orientation / Q000502:physiology*; D011235:Predatory Behavior / Q000502:physiology; D011892:Rana catesbeiana / Q000033:anatomy & histology* / Q000254:growth & development / Q000502:physiology; D013477:Superior Colliculi / Q000033:anatomy & histology / Q000254:growth & development* / Q000502:physiology; D014795:Visual Pathways / Q000033:anatomy & histology / Q000254:growth & development* / Q000502:physiology
Brain Res. 1984 Jan 9;290(2):219-38
6198041
Vis Neurosci. 1991 Nov;7(5):459-78
1764416
J Comp Neurol. 1983 Mar 1;214(3):321-32
6602152
J Neurosci. 1984 Jan;4(1):43-57
6198496
Neuroscience. 1995 Mar;65(1):119-60
7753394
J Comp Neurol. 1987 Mar 15;257(3):396-404
3558896
J Neurosci Methods. 1992 Oct-Nov;45(1-2):71-86
1283434
Brain Behav Evol. 2007;69(1):1-19
16912473
Brain Res. 1988 Aug 16;458(1):185-91
2463043
J Comp Neurol. 2005 Jun 27;487(2):127-46
15880498
J Comp Neurol. 1977 May 15;173(2):219-30
300743
J Hirnforsch. 1996;37(4):519-35
8982811
Brain Behav Evol. 1999;53(1):10-9
9858801
Exp Brain Res. 2003 Jul;151(1):123-35
12748838
J Comp Neurol. 1983 Mar 20;215(1):108-20
6602154
Exp Brain Res. 1982;47(3):394-406
6982173
Brain Behav Evol. 2002;60(1):36-51
12239469
J Comp Neurol. 1986 Jul 15;249(3):411-27
3734164
J Comp Neurol. 2005 Mar 21;483(4):437-57
15700277
Prog Brain Res. 2006;151:321-78
16221594
Brain Behav Evol. 1992;40(1):1-16
1393516
J Comp Neurol. 1982 Feb 20;205(2):139-52
7076889
Arch Histol Jpn. 1980 May;43(2):157-73
6998405
Anat Embryol (Berl). 1990;181(2):167-76
2327597
Nature. 1977 Sep 1;269(5623):54-6
895885
Brain Res. 1995 Mar 13;674(1):107-11
7773677
Neurosci Lett. 1982 Nov 30;33(2):107-13
7155452
J Comp Neurol. 1983 Jun 10;217(1):54-74
6603481
Neurosci Lett. 1985 Aug 5;58(3):365-70
3876526
J Comp Neurol. 1990 Jan 1;291(1):103-27
2298926
J Neurosci. 1985 Dec;5(12):3228-45
3001241
Behav Neurosci. 1987 Jun;101(3):378-84
3496901
J Comp Physiol A. 1995 Nov;177(5):577-90
7473306
J Comp Neurol. 1985 Feb 1;232(1):25-35
3973081
Brain Res. 2007 Jul 9;1157:23-31
17550783
J Neurosci. 1984 Feb;4(2):442-57
6607979
Proc Natl Acad Sci U S A. 1971 Mar;68(3):528-32
5276755
J Neurosci. 2007 Jan 24;27(4):782-90
17251417
Brain Res Dev Brain Res. 1993 Mar 19;72(1):21-39
7680968
Dev Neurobiol. 2009 Dec;69(14):959-71
19813244
Dev Psychobiol. 1988 May;21(4):383-95
3259939
Brain Behav Evol. 1988;32(4):208-19
3233482
J Neurosci Methods. 1992 Jan;41(1):31-43
1578900
Eur J Neurosci. 1997 Oct;9(10):2100-9
9421170
J Hirnforsch. 1990;31(3):337-40
2230102
J Neurophysiol. 2009 Dec;102(6):3392-404
19793878
Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14877-82
9405707
Brain Behav Evol. 1998;51(3):144-61
9519288
J Comp Neurol. 1983 May 20;216(3):319-26
6306067