Ontogeny of the tectorotundal pathway in chicks (Gallus gallus): birthdating and pathway tracing study

Abstract

The avian tectorotundal system has been suggested as a homologue of the mammalian colliculopulvinar system. In the tectorotundal system, neurons of the stratum griseum centrale (SGC) of the optic tectum send their axons bilaterally to the nucleus rotundus (Rt). In transit to the Rt, the axons of the SGC neurons collateralize in the nuclei posteroventralis thalami (PV), subpretectalis (SP), and interstitiopretectosubpretectalis (IPS) of the tectothalamic tract (TT). The current study used birthdating and pathway-tracing methods to investigate the neurogenesis and time course of neuronal connections of the tectorotundal pathway in chicks during embryogenesis. By using tritiated thymidine autoradiography, we observed that the SGC neurons of the tectum were generated by embryonic days 3.0-5.5 (E3.0-E5.5), the Rt by E3.5-E5.0, and the nuclei of TT by E3.5-4.5. To trace the tectorotundal pathway, we injected cholera toxin B subunit (CTb) into the tectum, and the CTb-like immunoreactivity was examined. By E4.5-E5.5, some CTb-like immunoreactive (CTb-LI) axons terminated in the ipsilateral SP/IPS. By E6.0-E6.5, CTb-LI axon bundles were seen ipsilaterally in the TT. Increased numbers of labeled axons were seen terminating in the SP/IPS. By E7.0-E7.5, heavily labeled axons in the TT were observed with diffuse terminals in areas ventral to the presumptive Rt and PV. By E7.5-E8.0, the tectal axons innervated the ipsilateral Rt, in which some of the collaterals crossed the midline to the contralateral diencephalon. The crossed tectorotundal projection was seen first by E8.0-E8.5. Also, during this stage, a few CTb-LI collaterals terminated in the contralateral SP/IPS. Between E10 and E13, the pattern of bilateral tectorotundal projections became more regionalized, whereas labeling continued to increase in the SP/IPS. At E16, the labeling pattern of all tectorecipient structures resembled that of the hatchling. The current study revealed the temporal order of development of the tectorotundal pathway during embryogenesis. The SGC cells first innervate ipsilaterally the SP/IPS and then the Rt/PV. The schedule of the crossed tectorotundal connections coincides with the schedule of tectal projections onto the contralateral intrinsic nuclei of the TT. We conclude that E8.0 (+/- E0.5) is a critical stage for the development of the tectofugal pathway. Moreover, the current study provides important insights into the relative ontogeny of the mammalian tectofugal pathway.