Acoustical Society of America
157th Meeting Lay Language Papers


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Two Ears are Better than One for Toadfish to Find Each Other

Peggy Edds-Walton - plewalton@yahoo.com
Neuroscience Institute
Marine Biological Laboratory
Woods Hole, MA 02543

Popular version of 1pABa
Presented on Monday afternoon, May 18, 2009
157th ASA Meeting, Portland, OR

Although you can’t see them from the outside of the fish, fish have ears. The paired ears lie inside the body, and they have much in common structurally with those of other vertebrates, although they lack the coiled hearing organ that mammals have (the cochlea). The part of the inner ear that “hears,” the auditory endorgan, encodes sound in the same way that the ears of other vertebrates do, but is also sensitive to the direction of the sound stimulus. The information about sound is sent from the auditory endorgan to a site in the hindbrain, and the hindbrain site sends information to a secondary site in the hindbrain and to a midbrain site, as in other vertebrates. The secondary hindbrain site is the first place where information from the left and the right ear is combined in most vertebrates. The comparison of left and right is necessary for sound source localization in terrestrial vertebrates. Sorting sounds by source is a basic function of the auditory system of all vertebrates. But do fish combine the input from both ears to determine the direction or do they use just one?

This study is part of a continuing analysis of the auditory system of a vocal fish to determine how basic auditory processing is conducted by the nervous system. A male toadfish produces sounds (“boatwhistle”) to attract females to his nest, mostly at dawn and dusk when light levels are very low. One of the research questions we have been investigating is “how does the female find the male using his sounds?”


LISTEN: Boatwhistle

My collaborator, Richard Fay, and I have determined the auditory circuit in toadfish using anatomical methods (Ref. 1, 2, 3), and we have determined how the nervous system encodes sound and direction in the ear (Ref. 4) and the brain (Ref. 5, 6) using physiological methods. Direction is encoded at all levels of the nervous system from the ear to the midbrain. In other words, there are cells at every level of the circuit that respond best to sounds from a particular direction and less well to sounds from other directions, with a null (no response) perpendicular to the best direction. We evaluate how a cell responds to sounds at 30 degree intervals in the horizontal and vertical planes and plot the data as a directional response pattern (DRP) for each cell. For example, a cell might respond very well to a 100 Hz sound that lies at 30 degrees to the left of the fish (with 0 degrees at the snout), but that same cell does not respond well to that same sound if it were located at 30 degrees to the right of the fish. We also found anatomical evidence that the information from the left and right ears may be combined at the first possible site in the hindbrain, unlike most other vertebrates. The name of that first site is the descending octaval nucleus (DON).

In order to figure out if left and right information is combined in the DON, we needed to record the directional response pattern from a cell on one side (left DON) and then remove or alter the input from the other side (right ear) to see if the physiological response to sound direction (the DRP) changed. If the DRP changes, that would tell us that information from both ears was being used to produce the DRP we recorded initially. To remove or alter the input from one side, an experimenter can cut the nerves to that ear, which is a permanent loss of input from that ear. Once the auditory nerve is cut, there can be no further search for cells with left and right inputs, and the experiment ends with only one trial. Alternatively, the experimenter could use an anesthetic to stop activity in the nerve from one ear. That is difficult to do consistently, and the effect is not immediate nor does it go away quickly. We discovered that we could easily alter the responses from an ear by tipping the critical structures in the ear to an abnormal angle, using a tiny glass probe. The tipping method was reversible and repeatable.

Using the tipping method, we confirmed that we could identify cells that received input from both left and right ears in the midbrain, which is consistent with other vertebrate auditory circuits. Then we confirmed that altering the orientation of the ear on the right side did indeed alter the DRP of cells in the left DON (Ref. 7). We could get different changes in the DRP, which indicated that the information from the two ears is added together or one is subtracted from the other. Therefore, we can conclude that the toadfish combines input from the left and right ear at the first possible site in the brain, unlike most other vertebrates. Furthermore, as we continue to evaluate how the fish’s brain puts together the information it receives from the ears to determine where a sound source is, we know that we must first understand the circuit that links the left and right DONs.

References
1. Edds-Walton, PL 1998. Hearing Research, 123:41-54.
2. Edds-Walton, PL, Fay, RR, and Highstein, SM. 1999. J. Comp. Neurol., 411:212-238.
3. Edds-Walton, PL and Fay, RR. 2005. Brain, Behavior, and Evolution, 66:73-87.
4. Fay, RR and Edds-Walton, PL. 1997. Hearing Research, 111:1-21.
5. Edds-Walton, PL and Fay, RR. 2005. J. Comp. Physiol. A, 191:1079-1086.
6. Edds-Walton, PL and Fay, RR. 2008. J. Comp. Physiol. A, 194:1013-1029.
7. Edds-Walton, PL and Fay, RR. 2009. J. Exper. Biol., in press.


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