The tradition of comparing the overall body plan of various organisms is ancient, dating back to the early scientists of the ancient civilizations. A resurgence occurred during the 17th
Century when naturalists in Britain and elsewhere began compiling drawings of diverse life forms (e.g. Samuel Collins; see Kruger 2004
). The more formal field of comparative neurobiology had its roots in the end of the 19th
Century with the early neuroanatomists including Cajal and Ariens Kappers. The field flourished in the early 1900’s in the hands of the Herricks, J. B. Johnston and their students. One of the key concepts pervading comparative neurobiology is that by letting nature perform the experiments of species and niche specializations, scientists can learn which features of a system are fundamental features common to many forms, and which traits are derived specializations or elaborations on the common plan. This paper describes one of the specializations on the bauplan of the gustatory system.
The sense of taste evolved in the earliest vertebrates. Taste buds, although absent in hagfish, can be recognized in lampreys, fishes including chondrichthyes, amphibians and amniotes. A key feature of the taste system is that taste buds are always innervated by one of the cranial nerves that contain ganglion cells derived from epibranchial placodes (CN VII: facial; CN IX glossopharyngeal; CN X: Vagus) (Barlow and Northcutt 1995
) although the taste bud cells themselves arise from the local epithelium (Barlow and Northcutt 1995
; Stone et al. 1995
In all vertebrates, the taste nerves enter the medulla to terminate within the visceral sensory column as described by Herrick (Herrick 1922
) and others. These nerves also carry general visceral information, e.g. from heart or gut, but the general visceral inputs terminate in separate, more caudal reaches of the visceral sensory column. This general pattern of organization occurs in all vertebrates and thus must be regarded as part of the overall “bauplan” of the brain.
In amniote vertebrates, the gustatory system is relatively staid and varies little across species. In contrast, the relative size and complexity of the gustatory system varies greatly between teleosts. At least 5 groups of fishes appear to have elaborated different types of complexities in this system all the while maintaining the basic bauplan.
This paper will focus on the highly elaborate vagal gustatory system in the common goldfish, Carassius auratus
. In goldfish and closely related carps, the brainstem nuclei serving vagal-mediated taste functions can occupy upwards of 20% of the total mass of the brain (Kotrschal and Palzenberger 1992
). This is clearly an important system in these species.
Casual observation of goldfish, as many of us do when we are children, admits of no obvious complex behaviors that may be served by such an elaborate neuronal machine. Indeed, my own initial observations of goldfish led me to the conclusion that they barely have any behavior whatsoever. If one sprinkles food along the top of the water, the fish pick off individual food particles, apparently using vision in a fashion similar to almost all other diurnal animals. But if one waits for the food to sink to the bottom, a more interesting and subtle behavior can be observed. The food tidbits mix in with the substrate – gravel, sand or mud. The fish orients head downward and vacuums up the mixture. The fish then manipulates the mix in the mouth, finally spitting out what was just taken in. Such is the appearance. But more careful observation shows that what the fish spits out is only the substrate; all the food has been retained. This task is tantamount to our placing a small candy into a handful of fine gravel and popping the whole handful into one’s mouth. The task then is to sort out the candy from the stones. We can do this, albeit slowly, and by using a serial consideration of each potential object in the mouth. Goldfish use a different strategy. In order to understand this behavior, it is necessary to understand the structure of the oral cavity of a goldfish. This description below is based on the elegant work of F. Sibbing (Sibbing et al. 1986
; Sibbing and Uribe 1985
) who used SEM and X-ray cinematography to study the oral cavity and food handling of a carp which is similar in structure and function to goldfish. A more recent work by Callan and Sanderson confirms and extends these findings (Callan and Sanderson 2003