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Sharpening of Directional Auditory Input in the Descending Octaval Nucleus of the Toadfish, Opsanus tau.

The investigation concerns the fate of acoustic directional encoding in the medulla of Opsanus tau. The descending octaval nucleus (DON) is the nucleus receiving the majority of auditory input from the saccule. Previous work has shown that saccular afferents encode directional auditory information that could be used to determine the location of a sound source (1, 2). Each saccular afferent projects to multiple sites along the rostral-caudal axis of the DON (3). Most saccular afferents show a cosinusoidal response pattern to motional stimuli in the horizontal and midsagittal planes (2). Recently, we reported that directional auditory responses were present in the DON (4). In this study, we examine directional response properties of cells in the DON that were sharpened compared to primary saccular afferents.

Prior to surgery, the toadfish was anesthetized lightly (3 aminobenzoic acid), and the tail muscles were paralyzed (pancuronium bromide). The dorsal surface of the cranium was removed to expose the left lateral surface of the medulla between the posterior ramus of the eighth cranial nerve ([VIII.sub.p]) and cranial nerve IX, near the rostral and mid-region of the DON, respectively. The fish's head was secured in a circular dish (containing seawater) that is mounted on a three-dimensional shaker table described in detail elsewhere (2). Minishakers produced sinusoidal, translatory motion of the dish in the horizontal and mid-sagittal planes at 30 [degrees] intervals. This stimulus simulates the particle motion component of underwater sound.

Extracellular recordings were made using woodsmetal-filled electrodes (4, 5), with 10-12 [[micro]meter] tip diameters and NaCl-filled capillary tubes with 5-7 [[micro]meter] tips and resistances of 3-8 m[Omega]. These electrodes produced comparable data. A three-axis micromanipulator was used to position the electrode, and recording sites were documented by noting micromanipulator position during recording. Neurobiotin was injected (4% in 2M NaCl, 1900-2000 nA for 10-20 min) once per animal at an auditory site. This procedure helped document recording location for use in future neuroanatomical analyses.

The 88 recordings made in the DON contain two categories of directional responses: primary-like and sharpened. Primary-like DON cells have cosinusoidal directional response patterns similar to those seen in saccular afferents (1, 2). Many cells recorded in the DON had directional response patterns that differed from simple cosine functions: they are sharpened [ILLUSTRATION FOR FIGURE 1A OMITTED] with torpedo-shaped patterns (63% of 88). Sharpened cells were further categorized as slightly (23%), moderately (28%), or highly (12%) sharpened based on the magnitude of their deviation from a cosine function. Some cells were sharpened in only one plane (n = 15, with only mid-sagittal plane sharpening in 11 cells, and only horizontal plane sharpening in 4 cells). The rest (n = 40) were sharpened in both planes to some extent. Although we cannot determine with certainty whether these recordings were made from primary afferent axons or from cells of the DON, response patterns classified as very sharpened or moderately sharpened (40%) were never observed in over 400 recordings from saccular afferents (2). Further work using intracellular recording and neurobiotin injection will help resolve this ambiguity.

Figure 1A illustrates directional response patterns of a representative sharpened DON cell in the horizontal plane. Sharpening is level-independent for this cell and results in a responsiveness maximum oriented about 30 [degrees] to the left front. Idealized cosine responsiveness functions are illustrated in Figure 1B. Clearly, the directional response of the DON cell is not well modeled by a single cosine function. The directional responses of most sharpened cells in the DON are well modeled by a combination of excitation and inhibition from at least two inputs with cosinusoidal directional response patterns. Fitting excitatory and inhibitory cosinusoidal influences to a cell's directional response function gives the relative magnitudes and orientations of the hypothetical inputs. For this cell, hypothetical excitatory and inhibitory magnitudes are approximately equal at all levels, with the excitatory cosine oriented at about 36 [degrees] to the left front, and the inhibitory cosine oriented at about 34 [degrees] to the right front. The origin of the putative inhibition remains to be determined, but could arise from the contralateral ear via commissural DON connections (6).

Research funded by a National Institutes of Health R01 grant to the Parmly Heating Institute.

Literature Cited

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: 1-21.

3. Edds-Walton, P. L., R. R. Fay, and S. M. Highstein. 1999. J. Comp. Neurol. 411(2): 212-238.

4. Edds-Walton, P. L., and R. R. Fay. 1998. Biol. Bull. 195: 191-192.

5. Dowben, R. M., and J. E. Rose. 1953. Science 118: 22-24.

6. Edds-Walton, P. L. 1998. Hear. Res. 123: 41-54.
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Author:Fay, R. R.; Edds-Walton, P. L.
Publication:The Biological Bulletin
Article Type:Brief Article
Geographic Code:1USA
Date:Oct 1, 1999
Words:775
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