Development of the Olfactory System in a Wallaby <i>(Macropus eugenii)</i>

Abstract

We used carbocyanine dye tracing techniques in conjunction with hematoxylin and eosin staining, immunohistochemistry for GAP-43, and tritiated thymidine autoradiography to examine the development of the olfactory pathways in early pouch young tammar wallabies (Macropus eugenii). The overarching aim was to test the hypothesis that the olfactory system of newborn tammars is sufficiently mature at birth to contribute to the guidance of the pouch young to the nipple. Although GAP-43 immunoreactive fibers emerge from the olfactory epithelium and enter the olfactory bulb at birth, all other components of the olfactory pathway in newborn tammars are very immature at birth, postnatal day (P0). In particular, maturation of the vomeronasal organ and its projections to the accessory olfactory bulb appears to be delayed until P5 and the olfactory bulb is poorly differentiated until P12, with glomerular formation delayed until P25. The lateral olfactory tract is also very immature at birth with pioneer axons having penetrated only the most rostral portion of the piriform lobe. Interestingly, there were some early (P0) projections from the olfactory epithelium to the medial septal region and lamina terminalis (by the terminal nerve) and to olfactory tubercle and basal forebrain. The former of these is presumably serving the transfer of LHRH⁺ neurons to the forebrain, as seen in eutherians, but neither of these very early pathways is sufficiently robust or connected to the more caudal neuraxis to play a role in nipple finding. Tritiated thymidine autoradiography confirmed that most piriform cortex pyramidal neurons are generated in the first week of life and are unlikely to be able to contribute to circuitry guiding the climb to the pouch. Our findings lead us to reject the hypothesis that olfactory projections contribute to guidance of the newborn tammar to the pouch and nipple. It appears far more likely that the trigeminal pathways play a significant role in this behavior because the central projections of the trigeminal nerve are more mature at birth in this marsupial.

The olfactory system of the tammar wallaby is developed at birth and directs the neonate to its mother's pouch odours

“…However, this sensory system is required only for a simple switch in direction so minimal development may be sufficient. Our behavioural observations disagree with the conclusions of Ashwell et al (2008) and show for the first time that the pouch young of the tammar wallaby is attracted to the odours from the mother's pouch (although our experiments did not assess the specificity of the behavioural response to odour). We conclude that both olfactory systems are capable of receiving odour signals at birth, a function that must be a critical adaptation for the survival of an altricial marsupial neonate such as the tammar for its journey to the pouch.…”

“…However, since the mother licks generally over the fur of the lower abdomen (Renfree et al 1989), rather than licking a specific track towards the pouch, this seems unlikely to provide much directional assistance to the young. Ashwell et al (2008) identified neural connections from the olfactory epithelium to the olfactory tubercle and basal forebrain but saw few connections past the olfactory bulb. They concluded that the olfactory system of newborn tammar is not sufficiently developed to play a role in guiding the young to the teat.…”

Early development of the nervous system of the eutherian &lt;i&gt;Tupaia belangeri&lt;/i&gt;

“…Thus, it turned out that, in newborn marsupials (Macropus eugenii), these pathways are usually too immature to support guidance to the pouch and nipple (Ashwell et al, 2008). Accordingly, at birth, the degree of maturity of these olfactory pathways is not high enough to allow olfaction-mediated behavior in platypus and echidnas, "two modern monotreme lineages that have followed independent evolutionary paths from a less olfaction-specialized ancestor" (Ashwell, 2012).…”

Development of the Vestibular Apparatus and Central Vestibular Connections in a Wallaby <i>(Macropus eugenii)</i>

“…After the remarkable climb to the pouch, other sensory inputs must guide the newborn in finding and attaching to the teat, possibly mediated through the trigeminal pathways and medial medullary reticular formation. Our recent work on olfactory development in this mammal indicate that olfaction is unlikely to play a role in teat-finding behavior [Ashwell et al, 2008]. Although the mechanisms enabling this remarkable independent journey in young marsupials are becoming clearer, discovering their full extent remains an exciting scientific endeavor.…”