ON THE PHYLOGENY AND MORPHOLOGICAL POSITION OF THE TERMINAL BUDS OF FISHES.1

By C. JUDSON HERRICK.

These curious sense organs occurring in the skin of certain fishes have been a source of perplexity and controversy among morphologists since their discovery by LEYDIG in 1851. They are found freely scattered over the surface of the skin of the head and trunk in certain teleostean and ganoidean fishes, particularly in exposed situations, and hence by many observers have been regarded as tactile organs. Indeed, MERKEL in 1880, having failed altogether to find the proper tactile nerves in the skin of fishes belonging to what we now designate as the general cutaneous system, supposed that these organs, together with the neuromasts or organs of the lateral line system, were developed in compensation for the absence of the typical free tactile nerve endings of the other vertebrates. This we now know to be wide of the mark, for all fishes which possess either or both of the systems of special sense organs mentioned above also possess in the same cutaneous areas an abundant general cutaneous nerve supply for tactile sensation.

We must distinguish at the outset three distinct types of sensory nerve endings in the skin of fishes and then inquire into their respective morphological rank; viz., (1) the general cutaneous nerve termini, (2) the neuromasts, or organs of the acustico-lateralis system of sense organs, (3) the terminal buds, or end-buds.

(1) The first type comprises the ordinary tactile nerves, making up the greater part of the spinal dorsal roots, but represented in certain ones only of the cranial nerves. They are

1 Studies from the Neurological Laboratory of Denison University, No. XVII.

free nerve endings in the skin without specialized sense organs and may be regarded as in all probability the most primitive type of sensory ending.

(2) Neuromasts. This system of sense organs includes the lateral canal organs, pit organs, ampullae and all other specialized organs associated with the lateral line canals and innervated by lateralis nerves, together with the sense organs of the internal ear of like phylogenetic origin and innervation. These organs clearly belong to a single system and the evidence thus far accummulated favors the inference that the system as a whole has been derived phylogenetically from the general cutaneous system of nerves. This is not the place to give the detailed proof of this, but the trend of the current argument may be summarized as follows under two heads :

(a) the sense organs themselves are characterized in their adult and highly functional condition by the presence of hair cells differentiated from indifferent supporting cells and extending only part way through the epithelium of the sense organ. These hair cells may not occur in the earliest embryological stages of development of the organs, nor in states of functional and structural degradation. The former point accounts for the statements of several authors to the effect that the lateral line organs pass through a developmental stage which is similar to the adult structure of the terminal buds, and the latter point for the confusion which has arisen in the minds of many. authors, giving rise to the belief that there is no clearly marked structural difference between neuromasts of the lateral line series and the terminal buds. Nevertheless, the distinction drawn by SCHULZE and MERKEL between the neuromasts and terminal buds, the former possessing the hair cells and the latter not, stands as an essential criterion in all cases where the organs are well developed. Now these hair cells resemble somewhat in structure and probably also in mode of function the tactile hairs of certain aquatic invertebrates and in fact are probably phylogetically derived from them. PARKER ('03) has shown clearly the probable line of differentiation of these structures from tactile organs for the perception of mass move

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ment of the water to organs of equilibration and hearing. therefore have structural and physiological evidence that the sense organs of the acustico-lateralis system have been derived from tactile organs.

(b) Now turning to the central connections of the acusticolateralis nerves within the brain, we have a quite independent line of evidence. It has long been known that these nerves all end in the tuberculum acusticum and associated centers, and it has recently been shown, particularly by JOHNSTON in an important series of papers, that these centers are all derivatives of the general cutaneous or tactile centers of the brain. While my own studies on the teleosts have shown that in these higher fishes the specialization of the acustico-lateralis centers has progressed so far as to obscure the primary relations, JOHNSTON'S Observations on the lower fishes leave no room for doubt that the history is as stated above.

From the concurrent history of both central and peripheral relations we are therefore justified in assuming that the neuromasts and their associated nervous apparatus have been derived from the general cutaneous or tactile system of nerves.

(3) The terminal buds (end-buds, beaker organs, etc.) are by no means on 30 secure a morphological foundation. It is, however, now definitely known that they resemble in every essential respect the taste buds within the mouth cavity. The specific sensory cells are not hair cells, but, like the indifferent supporting cells, they run through the entire thickness of the sensory epithelium from external to internal limiting membrane. They may terminate distally in a short stiff bristle, but never in the tuft of long hairs characteristic of hair cells. The organs usually rest on a raised papilla of dermis, and finally in every case where the innervation is accurately known they are supplied by communis nerves, which have nothing in common either centrally or peripherally with the general cutaneous or acustico-lateralis systems of nerves. On the other hand, these nerves always terminate within the brain in a single center (bilobed in some fishes), the vagal lobe (plus facial lobe in silur

oids and cyprinoids), which also receives the typical gustatory fibers from the taste buds of the mouth.

If now it can be shown that the terminal buds differ functionally, as well as in this thorough-going structural fashion, from all other cutaneous sense organs, then it would appear that their rank as a separate system of sense organs should remain unchallenged. And such in fact is the attitude of most of the recent students of this question, even without a rigid demonstration of the functional relations. I am, however, at this time in a position to contribute positive facts regarding the functions of the terminal buds, and since one recent author of note has within the year made a very forcible plea for a return to the older standpoint of LEYDIG and others that terminal buds and neuromasts are genetically related, I am moved to review the whole question again.

But first we must examine more thoroughly the central nervous connections of the terminal buds, since the morphological argument really hinges upon this point. I repeat, that the terminal buds of the outer skin of fishes are known to be innervated by a system of nerves which is entirely distinct throughout from either the tactile or lateralis nerves. There are no accurate observations which contradict this conclusion, while the positive evidence is quite decisive. The most convincing chapter in the elucidation of this problem is, I think, my own examination of the innervation of the cutaneous organs in Ameiurus (HERRICK, 'OI), which was undertaken primarily to test this very question. The cyprinoids would give an equally decisive answer to the problem, as I know from personal observation (as yet unpublished), though perhaps here the evidence would not be quite so easy to read.

The nerves from these terminal buds, no matter where they are located on the body, always reach the central nervous system through either the X, IX or VII pairs of cranial nerves, and so far as my personal observation goes, practically all come in by the VII nerve, though all three of these nerves in all types receive gustatory fibers from taste buds within the mouth. Both of these classes of fibers, together with a large number of

unspecialized visceral sensory fibers must be treated together within the brain, since they are so intimately intermingled that analysis has so far proven impossible. Accordingly, they are termed collectively the "communis system" of cranial nerve fibers. Peripherally this system is clearly divisible into two components, (1) the unspecialized visceral sensory which is doubtless much more ancient phylogenetically, and (2) the specialized, which for reasons to appear we may now term the gustatory component. This component may be divided topographically into two divisions, one for taste buds within the mouth, and one for terminal buds in the outer skin. It is the latter division only, of course, with which we are here concerned.

In fishes in which the terminal buds are not exceedingly numerous, as in the cod, their nerve fibers, though they enter the brain by the facial nerve, all turn back in the fasciculus communis to find their terminal nucleus in the vagal lobe, along with all other communis nerves of the body. But in the two groups of teleostean fishes in which these organs are most abundant (viz., the siluroids and cyprinoids) their nerve fibers find their terminal nucleus at the cephalic end of the fasc. communis in a special center, the lobus facialis. In both of these groups all of the terminal buds are innervated from the geniculate ganglion of the facialis root. Of this I am confident in the siluroids (HERRICK, 'OI). As to the cyprinoids, a rather cursory examination of sections of Carassius convinces me that the same is true, though my study of this type is not by any means exhaustive.

The facial lobe of the siluroids was formerly known as the lobus trigemini, that of the cyprinoids as the lobus impar, in the former case the structure being paired, in the latter unpaired by the fusion in the dorso-median line of the lobes of the two sides. That the facial lobes in these two groups of fishes are really merely differentiated parts of the vagal lobes is manifest, not only from the nature of their peripheral connections as indicated above, but still more evidently from their internal structure and secondary fiber connections. I can speak