Embed Size (px)
Citation preview
Sharpening of Directional Auditory Input in the Descending Octaval Nucleus of the Toadfish,Opsanus tauAuthor(s): R. R. Fay and P. L. Edds-WaltonSource: Biological Bulletin, Vol. 197, No. 2, Centennial Issue: October, 1899-1999 (Oct., 1999),pp. 240-241Published by: Marine Biological LaboratoryStable URL: http://www.jstor.org/stable/1542625 .
Accessed: 28/06/2014 09:07
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp
.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].
.
Marine Biological Laboratory is collaborating with JSTOR to digitize, preserve and extend access toBiological Bulletin.
http://www.jstor.org
This content downloaded from 141.101.201.171 on Sat, 28 Jun 2014 09:07:30 AMAll use subject to JSTOR Terms and Conditions
REPORTS FROM THE MBL GENERAL SCIENTIFIC MEETINGS REPORTS FROM THE MBL GENERAL SCIENTIFIC MEETINGS
Literature Cited 1. Marini, M., and I. Benedetti. 1992. Pp. 217-236 in Neurology
Today. I. Benedetti, B. Bertolini, and E. Capanna, eds. Selected Sym- posia and Monographs U.Z.I., 7, Mucchi, Modena.
2. Zottoli, S. J., E.-A. Seyfarth, C. J. Tyler, and D. S. Palmer. 1999. Neurosci. Abstr. 25: 104.
3. Sargent, P. E. 1899. Anat. Anz. 15: 212-225. 4. Bennett, M. V. L. 1960. Biol. Bull. 119: 303.
Literature Cited 1. Marini, M., and I. Benedetti. 1992. Pp. 217-236 in Neurology
Today. I. Benedetti, B. Bertolini, and E. Capanna, eds. Selected Sym- posia and Monographs U.Z.I., 7, Mucchi, Modena.
2. Zottoli, S. J., E.-A. Seyfarth, C. J. Tyler, and D. S. Palmer. 1999. Neurosci. Abstr. 25: 104.
3. Sargent, P. E. 1899. Anat. Anz. 15: 212-225. 4. Bennett, M. V. L. 1960. Biol. Bull. 119: 303.
5. Bennett, M. V. L., S. M. Crain, and H. Grundfest. 1959. J. Gen.
Physiol. 43: 221-250. 6. Bennett, M. V. L., Y. Nakajima, and G. D. Pappas. 1967. J. Neu-
rophysiol. 30: 161-179. 7. Barry, M. A., M. Weiser, R. Baker, and M. V. L. Bennett. 1986.
Biol. Bull. 171: 490-491. 8. Funakoshi, K., T. Kadota, Y. Atobe, M. Nakano, R. C. Goris, and
R. Kishida. 1998. Neurosci. Letters 258: 171-174.
5. Bennett, M. V. L., S. M. Crain, and H. Grundfest. 1959. J. Gen.
Physiol. 43: 221-250. 6. Bennett, M. V. L., Y. Nakajima, and G. D. Pappas. 1967. J. Neu-
rophysiol. 30: 161-179. 7. Barry, M. A., M. Weiser, R. Baker, and M. V. L. Bennett. 1986.
Biol. Bull. 171: 490-491. 8. Funakoshi, K., T. Kadota, Y. Atobe, M. Nakano, R. C. Goris, and
R. Kishida. 1998. Neurosci. Letters 258: 171-174.
Reference: Biol. Bull. 197: 240-241. (October 1999)
Sharpening of Directional Auditory Input in the Descending Octaval Nucleus of the Toadfish, Opsanus tau
R. R. Fay and P. L. Edds-Walton (Parmly Hearing Institute, Loyola University Chicago, Chicago, Illinois 60626)
Reference: Biol. Bull. 197: 240-241. (October 1999)
Sharpening of Directional Auditory Input in the Descending Octaval Nucleus of the Toadfish, Opsanus tau
R. R. Fay and P. L. Edds-Walton (Parmly Hearing Institute, Loyola University Chicago, Chicago, Illinois 60626)
This investigation concerns the fate of acoustic directional en-
coding 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 mid-
sagittal 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 ami-
nobenzoic acid), and the tail muscles were paralyzed (pancuro- nium 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 (VIIIp) 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 mo- tion of the dish in the horizontal and mid-sagittal planes at 30? intervals. This stimulus simulates the particle motion component of underwater sound.
Extracellular recordings were made using woodsmetal-filled electrodes (4, 5), with 10-12 g,m tip diameters and NaCl-filled
capillary tubes with 5-7 /um tips and resistances of 3-8 mfl. These electrodes produced comparable data. A three-axis micromanipu- lator was used to position the electrode, and recording sites were documented by noting micromanipulator position during record-
ing. 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 neuroana- tomical 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
This investigation concerns the fate of acoustic directional en-
coding 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 mid-
sagittal 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 ami-
nobenzoic acid), and the tail muscles were paralyzed (pancuro- nium 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 (VIIIp) 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 mo- tion of the dish in the horizontal and mid-sagittal planes at 30? intervals. This stimulus simulates the particle motion component of underwater sound.
Extracellular recordings were made using woodsmetal-filled electrodes (4, 5), with 10-12 g,m tip diameters and NaCl-filled
capillary tubes with 5-7 /um tips and resistances of 3-8 mfl. These electrodes produced comparable data. A three-axis micromanipu- lator was used to position the electrode, and recording sites were documented by noting micromanipulator position during record-
ing. 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 neuroana- tomical 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 (see Fig. 1A) 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
simple cosine functions: they are sharpened (see Fig. 1A) 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
A: 16 - DON A: 16 - DON
-30 -30
Front 0
Front 0
Cosine Excitation + Cosine Excitation +
B: MODEL
Front
B: MODEL
Front Cosine Inhibition .... Cosine Inhibition ....
30 30
-60 -60
-90 -90
-120 -120
-1 ou ---- iu-150 150 180 / 180
5, 10, 15, 20 dB re: 1 nm Excitation & Inhibition = o , ~ ?
-1 ou ---- iu-150 150 180 / 180
5, 10, 15, 20 dB re: 1 nm Excitation & Inhibition = o , ~ ?
Figure 1. A: Directional responses for cell 6 (animal I) at four iso-displacement levels in the horizontal plane in polar coordinates. The
angular axis is the orientation of linear translatory motion. The radial axis is response magnitude (the Z-statistic: Z = R2N, where R is vector
strength-a phase-locking metric (2), where 0 < R - 1, and N is the number of spikes recordedfor eight repetitions of a 500 ms sinusoid at 100 Hz). The circular axis indicates a Z value of 350. In this polar plot, each directional stimulus axis is represented on the circle in degrees with
respect to straight ahead (0?). For each stimulus axis, response magnitude (Z) was plotted twice (at the nominal axis angle, and at this angle plus 180?). Thus, the distance between the polar plot origin and the plotted points represent the value of Z at each stimulus axis. B: Hypothetical excitatory (solid lines, + symbol) and inhibitory (dotted lines) cosine-
shaped directional inputs to a DON cell. The amplitudes and orientations
of the inputs were adjusted to form a difference function (gray lines and D
symbols, negative values set to zero) closely modeling the directional
response in Figure lA for the 15 dB level. The difference function is also
plotted in Figure 1A, which overlaps the cell's response completely.
Figure 1. A: Directional responses for cell 6 (animal I) at four iso-displacement levels in the horizontal plane in polar coordinates. The
angular axis is the orientation of linear translatory motion. The radial axis is response magnitude (the Z-statistic: Z = R2N, where R is vector
strength-a phase-locking metric (2), where 0 < R - 1, and N is the number of spikes recordedfor eight repetitions of a 500 ms sinusoid at 100 Hz). The circular axis indicates a Z value of 350. In this polar plot, each directional stimulus axis is represented on the circle in degrees with
respect to straight ahead (0?). For each stimulus axis, response magnitude (Z) was plotted twice (at the nominal axis angle, and at this angle plus 180?). Thus, the distance between the polar plot origin and the plotted points represent the value of Z at each stimulus axis. B: Hypothetical excitatory (solid lines, + symbol) and inhibitory (dotted lines) cosine-
shaped directional inputs to a DON cell. The amplitudes and orientations
of the inputs were adjusted to form a difference function (gray lines and D
symbols, negative values set to zero) closely modeling the directional
response in Figure lA for the 15 dB level. The difference function is also
plotted in Figure 1A, which overlaps the cell's response completely.
240 240
This content downloaded from 141.101.201.171 on Sat, 28 Jun 2014 09:07:30 AMAll use subject to JSTOR Terms and Conditions
PISCINE NEUROBIOLOGY AND BEHAVIOR PISCINE NEUROBIOLOGY AND BEHAVIOR
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 injec- tion will help resolve this ambiguity.
Figure 1A illustrates directional response patterns of a repre- sentative sharpened DON cell in the horizontal plane. Sharpening is level-independent for this cell and results in a responsiveness maximum oriented about 30? to the left front. Idealized cosine
responsiveness functions are illustrated in Figure lB. Clearly, the directional response of the DON cell is not well modeled by a
single cosine function. The directional responses of most sharp- ened 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 co- sinusoidal influences to a cell's directional response function gives the relative magnitudes and orientations of the hypothetical inputs.
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 injec- tion will help resolve this ambiguity.
Figure 1A illustrates directional response patterns of a repre- sentative sharpened DON cell in the horizontal plane. Sharpening is level-independent for this cell and results in a responsiveness maximum oriented about 30? to the left front. Idealized cosine
responsiveness functions are illustrated in Figure lB. Clearly, the directional response of the DON cell is not well modeled by a
single cosine function. The directional responses of most sharp- ened 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 co- sinusoidal 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 ori- ented at about 36? to the left front, and the inhibitory cosine oriented at about 34? 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 Hearing 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.
For this cell, hypothetical excitatory and inhibitory magnitudes are approximately equal at all levels, with the excitatory cosine ori- ented at about 36? to the left front, and the inhibitory cosine oriented at about 34? 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 Hearing 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.
Reference: Biol. Bull. 197: 241-242. (October 1999)
Acoustic Behavior and Reproduction in Five Species of Corydoras Catfishes (Callichthyidae) Ingrid M. Kaatz and Phillip S. Lobel (Boston University Marine Program,
Marine Biological Laboratory, Woods Hole, Massachusetts 02543)
Reference: Biol. Bull. 197: 241-242. (October 1999)
Acoustic Behavior and Reproduction in Five Species of Corydoras Catfishes (Callichthyidae) Ingrid M. Kaatz and Phillip S. Lobel (Boston University Marine Program,
Marine Biological Laboratory, Woods Hole, Massachusetts 02543)
Many catfishes produce stridulation and swimbladder sounds when disturbed (1, 2, 3, 4, 5, 6), although the role of catfish sound
production in intraspecific contexts has not been widely studied (7, 8). Males of the neotropical catfish Corydoras paleatus are known to produce agonistic and courtship stridulation sounds when re-
productively active (9). Catfish stridulation sounds are produced by microscopic bony ridges located on the distal end of the
pectoral fin spine that are rubbed against the wall of the spinal fossa (3). In Corydoras, these ridges are narrower and more acute than in other catfishes (4). Identifying a species' acoustic repertoire (i.e., the full range of contexts in which sound is produced) and if or how sounds differ is a necessary first step in understanding how a species communicates (10). To further describe the acoustic
repertoire of Corydoras catfishes, we conducted a study of five
species in aquaria. Our objectives were to determine (1) the be- havioral context for sound production, and (2) whether acoustic
activity levels (numbers and types of sounds) differed when the same fishes were reproductively and non-reproductively active.
Individual fishes (n = 122) were obtained through the pet trade as juveniles and raised to sexual maturity. The mean number of individuals per group was 10 (range 3-15). C. paleatus juveniles were born in captivity while others were wild caught. All fishes were similar in length and weight. Five species (10 groups) were
kept in 20-gallon aquaria in a soundproof room (Acoustic Systems Inc.). The acoustic behavior of adults was monitored using a
hydrophone (BioAcoustics Inc., frequency response 10-3000 Hz, sensitivity at 10 psi of -162 dBv//uPa ? 2.0 dB) and amplifier- speaker (frequency response 100 Hz-10,000 Hz). The average monitoring time for each species was 10 months (range 6-15 months). Sounds were recorded on videotape with a Panasonic
Many catfishes produce stridulation and swimbladder sounds when disturbed (1, 2, 3, 4, 5, 6), although the role of catfish sound
production in intraspecific contexts has not been widely studied (7, 8). Males of the neotropical catfish Corydoras paleatus are known to produce agonistic and courtship stridulation sounds when re-
productively active (9). Catfish stridulation sounds are produced by microscopic bony ridges located on the distal end of the
pectoral fin spine that are rubbed against the wall of the spinal fossa (3). In Corydoras, these ridges are narrower and more acute than in other catfishes (4). Identifying a species' acoustic repertoire (i.e., the full range of contexts in which sound is produced) and if or how sounds differ is a necessary first step in understanding how a species communicates (10). To further describe the acoustic
repertoire of Corydoras catfishes, we conducted a study of five
species in aquaria. Our objectives were to determine (1) the be- havioral context for sound production, and (2) whether acoustic
activity levels (numbers and types of sounds) differed when the same fishes were reproductively and non-reproductively active.
Individual fishes (n = 122) were obtained through the pet trade as juveniles and raised to sexual maturity. The mean number of individuals per group was 10 (range 3-15). C. paleatus juveniles were born in captivity while others were wild caught. All fishes were similar in length and weight. Five species (10 groups) were
kept in 20-gallon aquaria in a soundproof room (Acoustic Systems Inc.). The acoustic behavior of adults was monitored using a
hydrophone (BioAcoustics Inc., frequency response 10-3000 Hz, sensitivity at 10 psi of -162 dBv//uPa ? 2.0 dB) and amplifier- speaker (frequency response 100 Hz-10,000 Hz). The average monitoring time for each species was 10 months (range 6-15 months). Sounds were recorded on videotape with a Panasonic
VHS recorder (professional/industrial model AG-180, frequency response 100-8000 Hz).
The behavioral context for each sound produced was determined
by observing behavior, beginning with feeding, at night using a red
light. The mean number of hours sampled per species was 50 (19-77). Five species (C. aeneus, C. arcuatus, C. leopardus, C. paleatus, C. reticulatus) were stimulated into reproductive activity by simulating a tropical freshwater rainy season (6). For reproduc- tive fishes, the total number of 1-h samples was 81 and the mean number of hours sampled per species was 10 (6-25). Groups were maintained in non-reproductive condition by using a dry-season simulation (6). For non-reproductive fishes, the total number of 1-h
samples was 171 and the mean number of hours sampled per species was 34 (5-63). Chi-square was used to test for differences in sound production between reproductive and non-reproductive fishes for all groups and samples. Student's t test was used to
compare acoustic activity immediately preceding and following spawning for five groups that each had more than 10 individuals per group.
The software package SIGNAL (Engineering Systems Inc., Bel- mont, MA) was used to determine total pulse number and fre-
quency range. These acoustic parameters are believed to be of
significance to fishes in intraspecific contexts (7, 8). A minimum of 40 courtship sounds per species were analyzed for determining pulse number for C. aeneus, C. leopardus, and C. paleatus (177 sounds total). A minimum of 30 sounds per species for agonistic chase sounds were analyzed for the same three species (90 total). A minimum of 6 agonistic pre-chase sounds were analyzed for C. arcuatus and C. reticulatus (total 18). For startle sounds, a mini- mum of three sounds were analyzed for C. leopardus and C. aeneus (8 total).
VHS recorder (professional/industrial model AG-180, frequency response 100-8000 Hz).
The behavioral context for each sound produced was determined
by observing behavior, beginning with feeding, at night using a red
light. The mean number of hours sampled per species was 50 (19-77). Five species (C. aeneus, C. arcuatus, C. leopardus, C. paleatus, C. reticulatus) were stimulated into reproductive activity by simulating a tropical freshwater rainy season (6). For reproduc- tive fishes, the total number of 1-h samples was 81 and the mean number of hours sampled per species was 10 (6-25). Groups were maintained in non-reproductive condition by using a dry-season simulation (6). For non-reproductive fishes, the total number of 1-h
samples was 171 and the mean number of hours sampled per species was 34 (5-63). Chi-square was used to test for differences in sound production between reproductive and non-reproductive fishes for all groups and samples. Student's t test was used to
compare acoustic activity immediately preceding and following spawning for five groups that each had more than 10 individuals per group.
The software package SIGNAL (Engineering Systems Inc., Bel- mont, MA) was used to determine total pulse number and fre-
quency range. These acoustic parameters are believed to be of
significance to fishes in intraspecific contexts (7, 8). A minimum of 40 courtship sounds per species were analyzed for determining pulse number for C. aeneus, C. leopardus, and C. paleatus (177 sounds total). A minimum of 30 sounds per species for agonistic chase sounds were analyzed for the same three species (90 total). A minimum of 6 agonistic pre-chase sounds were analyzed for C. arcuatus and C. reticulatus (total 18). For startle sounds, a mini- mum of three sounds were analyzed for C. leopardus and C. aeneus (8 total).
241 241
This content downloaded from 141.101.201.171 on Sat, 28 Jun 2014 09:07:30 AMAll use subject to JSTOR Terms and Conditions
