PART III. AUDITORY REACTIONS OF FROGS.

X. HEARING IN THE FROG.

A. Influences of Sounds in the Laboratory.

After determining the simple reaction time of the green frog to tactual and electrical stimulation, I attempted to do the same in case of auditory stimuli. In this I was unsuccessful because of failure to get the animal to give a motor response which could be recorded. The animal was placed in an experimenting box with a string attached to one hind leg as in the experiments described in Part II., and after it had become accustomed to the situation a sound was made. A wide range of sounds were tried, but to none except the croak of another frog was a motor reaction frequently given. Even a loud noise, such as the explosion of a large pistol cap, caused a visible motor reaction only in rare cases. In fifty trials with this stimulus I succeeded in getting three reactions, and since all of them measured between 230 and 240[sigma] it is perhaps worth while to record the result as indicative of the auditory reaction time. As these were the only measurements obtained, I have no satisfactory basis for the comparison of auditory with other reaction times.

The remarkable inhibition of movement shown by the frog in the presence of strong auditory stimulation, at least what is for the human being a strong stimulus, led me to inquire concerning the limits and delicacy of the sense of hearing in frogs. In the vast quant.i.ty of literature on the structure and functions of the sense organs of the animal I have been able to find only a few casual remarks concerning hearing.

In approaching the problem of frog audition we may first examine the structure of the ear for the purpose of ascertaining what sounds are likely to affect the organ. There is no outer ear, but the membrana tympani, or ear drum, covered with skin, appears as a flat disc from 5 to 10 mm. in diameter on the side of the head just back of the eye and a little below it. In the middle ear there is but one bone, the columella, forming the connecting link between the tympanum and the internal ear. The inner ear, which contains the sense organs, consists of a membranous bag, the chief parts of which are the utriculus, the sacculus, the lagena, and the three semicircular ca.n.a.ls. The cavity of this membranous labyrinth is filled with a fluid, the endolymph; and within the utriculus, sacculus and lagena are ma.s.ses of inorganic matter called the otoliths. The auditory nerve terminates in eight sense organs, which contain hair cells. There is no cochlea as in the mammalian ear. The a.s.sumption commonly made is that vibrations in the water or air by direct contact cause the tympanic membrane to vibrate; this in turn causes a movement of the columella, which is transmitted to the perilymphatic fluid of the inner ear. The sensory hair cells are disturbed by the movements of the otoliths in the endolymph, and thus an impulse is originated in the auditory nerve which results in a sensation more or less resembling our auditory sensation. It is quite probable that the frog's sense of hearing is very different from ours, and that it is affected only by gross air vibrations. This conclusion the anatomy of the ear supports.

Although there does not seem to be a structural basis for a delicate sense of hearing, one must examine the physiological facts at hand before concluding that frogs do not possess a sense of hearing similar to our own. First, the fact that frogs make vocal sounds is evidence in favor of the hearing of such sounds at least, since it is difficult to explain the origin of the ability to make a sound except through its utility to the species. Granting, however, that a frog is able to hear the croaks or pain-screams of its own species, the range of the sense still remains very small, for although the race of frogs makes a great variety of sounds, any one species croaks within a narrow range.

Having satisfied myself that motor reactions for reaction-time measurements could not be gotten to any ordinary sounds in the laboratory, I tried the effect of the reflex croaking of another frog of the same species. In attempting to get frogs to croak regularly, I tested the effect of removing the brain. The animals are said to croak reflexly after this operation whenever the back is stroked; but for some reason I have never been successful in getting the reaction uniformly. In many cases I was able to make normal animals croak by rubbing the back or flanks, and to this sound the animals under observation occasionally responded by taking what looked like an att.i.tude of attention. They straightened up and raised the head as if listening. In no case have other motor responses been noticed; and the above response was so rare that no reaction-time measurements could be made.

Again, while working with the green frog on habit formation, I one day placed two animals in a labyrinth from which they could escape by jumping into a tank of water. Several times when one frog jumped into the water I noticed the other one straighten up and hold the 'listening' or 'attentive' att.i.tude for some seconds. As the animals could not see one another this is good evidence of their ability to hear the splash made by a frog when it strikes the water.

B. Influence of Sounds in Nature.

In order to learn how far fear and artificial conditions were causes of the inhibition of response to sounds in the laboratory, and how far the phenomenon was indicative of the animal's inability to perceive sounds, I observed frogs in their native haunts.

By approaching a pond quietly, it is easy to get within a few yards of frogs sitting on the banks. In most cases they will not jump until they have evidence of being noticed. Repeatedly I have noted that it is never possible to get near to any frogs in the same region after one has jumped in. In this we have additional proof that they hear the splash-sound. To make sure that sight was not responsible for this on-guard condition in which one finds the frogs after one of their number has jumped into the water, I made observations on animals that were hidden from one another. The results were the same. I therefore conclude that the splash of a frog jumping into the water is not only perceived by other frogs in the vicinity, but that it is a peculiarly significant sound for them, since it is indicative of danger, and serves to put them 'on watch.'

A great variety of sounds, ranging in pitch from a low tone in imitation of the bull frog's croak to a shrill whistle, and in loudness from the fall of a pebble to the report of a pistol, were tried for the purpose of testing their effects upon the animals in their natural environment. To no sound have I ever seen a motor response given. One can approach to within a few feet of a green frog or bull frog and make all sorts of noises without causing it to give any signs of uneasiness. Just as soon, however, as a quick movement is made by the observer the animal jumps. I have repeatedly crept up very close to frogs, keeping myself screened from them by bushes or trees, and made various sounds, but have never succeeded in scaring an animal into a motor response so long as I was invisible. Apparently they depend almost entirely upon vision for the avoidance of dangers.

Sounds like the splash of a plunging frog or the croak or pain-scream of another member of the species serve as warnings, but the animals do not jump into the water until they see some sign of an unusual or dangerous object. On one occasion I was able to walk to a spot where a large bull frog was sitting by the edge of the water, after the frogs about it had plunged in. This individual, although it seemed to be on the alert, let me approach close to it. I then saw that the eye turned toward me was injured. The animal sat still, despite the noise I made, simply because it was unable to see me; as soon as I brought myself within the field of vision of the functional eye the frog was off like a flash.

Many observers have told me that frogs could hear the human voice and that slight sounds made by a pa.s.ser-by would cause them to stop croaking. In no case, however, have such observers been able to a.s.sert that the animals were unaffected by visual stimuli at the same time. I have myself many times noticed the croaking stop as I approached a pond, but could never be certain that none of the frogs had seen me.

It is a noteworthy fact that when one frog in a pond begins to croak the others soon join it. Likewise, when one member of such a chorus is frightened and stops the others become silent. This indicates that the cessation of croaking is a sign of danger and is imitated just as is the croaking. There is in this fact conclusive evidence that the animals hear one another, and the probability is very great that they hear a wide range of sounds to which they give no motor reactions, since they do not depend upon sound for escaping their enemies.

The phenomenon of inhibition of movement in response to sounds which we have good reason to think the frogs hear, and to which such an animal as a turtle or bird would react by trying to escape, is thus shown to be common for frogs in nature as well as in the laboratory.

This inhibition is in itself not surprising, since many animals habitually escape certain of their enemies by remaining motionless, but it is an interesting phenomenon for the physiologist. We have to inquire, for instance, what effects sounds which stimulate the auditory organs and cause the animal to become alert, watchful, yet make it remain rigidly motionless, have on the primary organic rhythms of the organism, such as the heart-beat, respiration, and peristalsis.

It is also directly in the line of our investigation to inquire how they affect reflex movements, or the reaction time for any other stimulus--what happens to the reaction time for an electrical stimulus, for example, if a loud noise precede or accompany the electrical stimulus.

For the purpose of determining the range of hearing in the frog, I was driven to study the influence of sounds upon respiration. Although the animals did not make any detectable movement, not even of an eyelid, in response to noises, it seemed not improbable that if the sounds acted as auditory stimuli at all, they would in some degree modify the form or rate of the respiratory movement.

C. Influence of Sounds on Respiration.[16]

[16] For full discussion of the normal respiratory movements of the frog see Martin, _Journal of Physiology,_ Vol. 1., 1878, pp. 131-170.

The method of recording the respiration was the direct transference of the movement of the throat by means of a pivoted lever, one end of which rested against the throat, while the other served as a marker on a revolving drum carrying smoked paper. The frog was put into a small box, visual stimuli were, so far as possible, excluded and the lever was adjusted carefully; a record was then taken for at least half a minute to determine the normal rate of respiration in the absence of the stimulus whose effect it was the chief purpose of the experiment to discover. Then, as soon as everything was running smoothly, the auditory stimulus was given. The following records indicate the effects of a few stimuli upon the rate of breathing:

1. Stimulus, 100 V. tuning fork.

Number of respirations for 10 cm. _before_ stimulus 18.0, 17.0; number of respirations for 10 cm. _after_ stimulus 19.0, 17.3.

The records indicate very little change, and contradict one another.

For the same stimulus the experiment was tried of taking the normal respiration record for a complete revolution of the drum, and then at once taking the record for the same length of time (about two minutes) with the tuning-fork vibrating close to the frog. The following result is typical and proves that the sound has little effect.

Number of respirations in a revolution _before_ stimulus: First rev.

88; second rev. 88. Number of respirations in a revolution _during_ stimulus: First rev. 87; second rev. 88.

Concerning the influence of tuning-fork stimuli more will be said later in a consideration of the effects of auditory stimuli upon reactions to visual stimuli.

2. The influence of falling water as an auditory stimulus. Water was allowed to fall about two feet in imitation, first, of a plunging frog, and second, of water falling over rocks. In representing the effect of the stimulus on the rate of respiration, I have given the distance on the drum covered by the ten complete respirations just preceding the stimulus and the ten following it.

10 Respirations. 10 Respirations.

_Before_ Stimulus. _After_ Stimulus.

1st Stim. 13.0 cm. 11.8 cm.

2d Stim. 12.7 cm. 12.7 cm.

With a smaller animal.

1st Stim. 5.4 cm. 4.8 cm.

2d Stim. 4.9 cm. 4.7 cm.

Average for 5 5.00 cm. 4.86 cm.

_These records show a marked increase in the rate of respiration just after the auditory stimulus is given for the first time._ The stimulus has less effect when repeated after an interval of one or two minutes, and if repeated several times it finally causes no noticeable change.

On the whole, the sound of falling water seems to arouse the animals to fuller life. The stimulus appears to interest them, and it certainly accelerates respiration. This is precisely what one would expect from a sound which is of special significance in the life of the animal.

3. In case of a loud shrill whistle inhibition of respiration resulted. This probably means that the frogs were frightened by the sound. Falling water served rather to excite their natural-habitat a.s.sociations, whereas, the whistle, being an uncommon and una.s.sociated sound, caused fear. It is evident to the casual observer that the frog sometimes inhibits and sometimes increases its respiratory movements when frightened, so the result in this experiment is in no way surprising. I am by no means certain, however, that a longer series of observations on several individuals would give constant inhibitory results. My immediate purpose in the work was to get evidence of hearing; the respiratory changes were of secondary importance, although of such great interest that I have planned a more thorough special study of them for the future.

A few sample results showing the influence of the whistle upon a small bull-frog follow:

Length of 10 Resps. Length of 10 Resps.

_Before_ Stimulus in cm. _After_ Stimulus in cm.

1st Stim. 6.0 6.7 2d " 5.4 6.0 3d " 5.9 5.8 1st " 4.7 5.4 2d " 4.4 4.6

As a test-check observation for comparison, the influence of a visual stimulus upon respiration was noted under the same conditions as for the auditory. Effect of turning on electric light over box.

Length in cm. of 10 Resps. Length in cm. of 10 Resps.

_Before_ Stimulus. _After_ Stimulus.

4.8 4.4 5.3 4.6 4.5 4.0

These results indicate an increase in the respiration rate due to the visual stimulus.

4. Of the other auditory stimuli used, the pistol-cap explosion gave very irregular results. For one animal it caused acceleration, for another inhibition. There is, however, good evidence that the sounds were heard.