Directional auditory responses in the descending octaval nucleus of the toadfish (Opsanus tau).
recordings (1,2). In this study, we have begun to characterize the response properties of one of the target nuclei of saccular afferents: the descending octaval nucleus (DON) (3,4). The DON has an extensive rostral-caudal distribution in the lateral medulla between the entrances of the anterior ramus of cranial nerve VIII and cranial nerve X [ILLUSTRATION FOR FIGURE 1A OMITTED]. In horizontal section, the nucleus is wedge-shaped with greatest width rostrally in the "dorsal zone" above the descending tract of cranial nerve V. Saccular afferents project most heavily to the dorsal zone of the descending octaval nucleus (dDON) (3,4).
Incoming saccular afferent fibers travel the length of dDON laterally, and terminal fields from those fibers are seen medial and lateral to the main axon (unpubl. obs.). Individual neurobiotin-filled cells revealed that all primary auditory axons branch repeatedly in the rostral-caudal axis of the dDON; however, variation was seen in the lateral to medial extent of terminal fields among afferents with different best elevations and best azimuths. Therefore, the goal of this preliminary study was to evaluate directional responsiveness across the lateral to medial axis of the dDON.
In preparation for the experiments, the toadfish was anesthetized and the tail muscles paralyzed. An incision was made in the dorsal surface of the skull, and the medulla was exposed carefully. The fish's head was then secured in a cylindrical dish filled with fresh seawater on a three dimensional shaker table. A system of moving-coil shakers created a sinusoidal motion of the dish along linear pathways (5). A calibration program produced the appropriate starting phases and amplitudes to create movements in the horizontal and mid-sagittal planes (0 [degrees], 30 [degrees] , 60 [degrees] , 90 [degrees] , 120 [degrees] , 150 [degrees]). Movement of the dish simulated the particle motion component of underwater sound at 100 Hz, a frequency to which the toadfish is extremely sensitive (5).
Extracellular recordings were made with indium electrodes designed for use in the central nervous system (6). The electrode tips were approximately 12 [[micro]meter] in diameter, which enhanced the likelihood that the electrodes were recording activity from secondary cell bodies in the dDON; recordings from axon collaterals or their terminal fields are not likely to be made with a large electrode tip. Multiple recordings were made in the same fish whenever possible; e.g., beginning laterally and moving medially on successive electrode penetrations. A three-axis micromanipulator was used to systematically change electrode position. Drawings were made to show electrode locations relative to VIII rami and IX in the rostro-caudal axis, and relative to the lateral edge of the brain and a large blood sinus that runs medially along the length of the medulla. Although "0" readings on the vertical scale of the micromanipulator were made at the surface of the medulla, the relative depth of the electrode was difficult to control at consecutive recording sites due to the curvature of the medulla. In some cases, a lesion was produced at the site of the last cell recorded to confirm our location in the dDON.
We have recorded more than 50 single units from the dDON in seven toadfish. We believe that the units are secondary cells of the dDON based on their response characteristics and the consistency of the data that we have recorded independent of location in the dDON. Although the dDON cells show phase-locking to the 100 Hz sinusoid, spikes are not produced for each cycle, which is unlike the regular phase-locked spiking patterns we have recorded from over 400 primary afferents. In addition, the activity of cells recorded at lateral sites does not differ from the activity of cells in the most medial locations of dDON. Recording from the small primary axon collaterals and terminal fields found medially would be extremely difficult with this large electrode. Secondary cell bodies in both lateral and medial locations are the most likely sources of the activity we have recorded.
Thirty-seven of the dDON units were phase-locked to the 100 Hz sinusoidal stimuli with root mean square displacement amplitudes between 10 and 30 dB (re 1 nm) and were clearly directional. The "best" axis for each cell was determined by plotting the cell's response to the six different angles of stimulation in each plane at three displacement amplitudes. All but one unit showed a directional response pattern with a consistent best axis of greatest phase-locked response, and an orthogonal "null" axis of minimal response in both the horizontal and midsagittal planes. These data indicate that the directional encoding among individual primary afferents is maintained at the level of the dDON, and the dDON may be a site of directional sound analyses.
The data collected from six cells in the dDON of a single fish are plotted by their relative locations in Figure 1. A portion of the dDON is represented in a horizontal section. Best elevation [ILLUSTRATION FOR FIGURE 1A OMITTED] and best azimuth [ILLUSTRATION FOR FIGURE 1B OMITTED] are shown separately for each cell at the appropriate relative location. Following our first successful recording, the micromanipulator was used to change the position of the electrode in the lateral-medial axis with no change in the electrode's location in the rostral-caudal axis. In some fish, such as the one illustrated in Figure 1, a second lateral to medial series of recordings was successful at a second more caudal (or more rostral) site.
We were able to obtain best elevations and best azimuths in consecutive lateral to medial sites in seven fish (37 cells). A comparison of the most lateral sites with the most medial sites indicated that elevation and azimuth vary widely along that axis of the dDON. For example, the range of best elevations most laterally was 0-90 [degrees] (n = 14 cells); the range of best elevations most medially was 0-95 [degrees] (n = 13 cells). The remaining ten cells were located between a most lateral and a most medial site; the range of best elevations at those sites was 0-45 [degrees] .
To our knowledge, this is the first study to show directional auditory responses in the dDON. Our future research will explore directional response properties along all three axes of the dDON (lateral-medial, rostral-caudal, dorsal-ventral) to determine whether direction is mapped systematically in this nucleus.
Research funded by a National Institutes of Health, RO1 grant.
1. Edds-Walton, P. L., and R. R. Fay. 1995. Biol. Bull. 189:211 212.
2. Fay, R. R., and P. L. Edds-Walton. 1997. Hear. Res. 111: 121.
3. Highstein, S.M., R. Kitch, J. Carey, and R. Baker. 1992. J. Comp. Neurol. 319: 501-518.
4. Edds-Walton, P. L. 1998. Hear. Res. 115: 45-60.
5. Fay, R. R., and P. L. Edds-Walton. 1997. Hear. Res. 113: 235-246.
6. Dowben, R. M., and J. E. Rose. 1953. Science 118: 22-24.
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|Author:||Edds-Walton, P.L.; Fay, R.R.|
|Publication:||The Biological Bulletin|
|Date:||Oct 1, 1998|
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