- Email: [email protected]
Small neurons in the vestibular nerve root project to the marginal shell of the anteroventral cochlear nucleus in the cat
BRAIN RESEARCH ELSEVIER
Brain Research 700 (1995) 295-298
Short communication
Small neurons in the vestibular nerve root project to the marginal shell of the anteroventral cochlear nucleus in the cat H.B. Zhao, K. Parham, S. Ghoshal, D.O. Kim * Division of Otolaryngology, Surgical Research Center, Department of Surgery and Neuroscience Program, UniL,ersity of Connecticut Health Center, Farmington, CT06030-1110, USA Accepted 16 August 1995
Abstract
We injected biotinylated dextran amine (BDA) into marginal shell regions of the anteroventral cochlear nucleus (AVCN) of the cat. These injections led to retrograde labeling of cells including small cells (median soma area = 111 /xm 2, equivalent diameter = 11.9/xm) in the vestibular nerve root (VNR), just ventral to an anterior part of the AVCN. This is an unexpected new finding. The cells were scattered among BDA-labeled fibers and were oriented parallel to the course of the VNR fibers. We suggest that the small neurons of the VNR might serve as second-order vestibular neurons conveying information from vestibular end organs to the cochlear nucleus (CN) and/or act as interneurons between the olivocochlear fibers in the VNR and the CN. Keywords: Small cell cap; Granule cells; Auditory brain stem; Biotinylated dextran amine; Retrograde transport; Olivocochlear fibers
The ventral cochlear nucleus (VCN) has a surrounding shell of granule cells and small cells [1,12,13]. A number of studies identified projections from a variety of origins to anteroventral cochlear nucleus (AVCN) marginal regions, including type II spiral ganglion cells [3], type I spiral ganglion cells physiologically characterized by low spontaneous rates [10], collaterals of the medial olivocochlear fibers [4], dorsal column nuclei [7,14] and primary vestibular afferent fibers [6,8]. Since the marginal shell of the VCN was not the focus of the above cited studies, the connections of this region remain largely unexplored. We used a complimentary approach of depositing a tracer into the region to identify sources of inputs. The left CN of the cat was exposed. The tracer-filled micropipette, 10% biotinylated dextran amine (BDA) (Molecular Probes) in 0.9% saline, was lowered into the CN. A focal injection ( < 100 nl) of the tracer was made using a Picospritzer (General Valve Co.). The cat survived for 7 - 8 days and transcardially perfused. B D A was visualized with avidin-biotin-peroxidase complex (ABC) histochemistry (Vector Laboratories) [15]. The extent of the BDA injection site was defined by the presence of extracellular BDA. Quantitative measurements of cell area and
* Corresponding author. E-maih [email protected]. 0006-8993/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved
SSD1 0 0 0 6 - 8 9 9 3 ( 9 5 ) 0 1 0 7 8 - 5
diameter were obtained using a computerized system (MicroBrightField Neurolucida). Injection of B D A into the marginal shell of the A V C N (Fig. 1A) resulted in labeling of small cells and fibers scattered throughout the body of the vestibular nerve root (VNR), just ventral to an anterior region of the A V C N and central to the Schwann cell-glial border of the vestibular nerve (VN) (Fig. 1B). Although these injections also labeled cell bodies and fibers in other parts of the brain, the present report is restricted to the VNR as outlined in Fig. lB. When the focal injection sites were primarily restricted to the granule cell layer (GCL) minimally extending into the small cell cap (SCC) (Q45, Fig. 1A; Q37, not shown), few or no labeled cells were found in the VNR (Table 1). When the injection sites included the SCC and little involved the lateral margins of the PD and PV areas of the A V C N (Q30 and Q28, Fig. 1A; Q39, not shown), there were substantially more labeled cells in the VNR (Table 1). When injection sites were placed in the A V C N core (cat Q34) or deep dorsal CN (DCN) (cat Q33), with little infringement on the marginal regions of the AVCN, no labeled cells were found in the VNR (Table 1). The cell bodies of the labeled cells in the VNR were spindle-shaped or ovoid (Fig. 1C). The dendrites of the labeled cells were usually visible, often including a few branches, and were parallel to the vestibular afferent fibers.
296
H.B. Zhao et al. / Brain Research 700 (1995) 295-298
Dot.
cat# Q30 ~ , / GCL~/~
eat# Q28
cat# Q45
i
GCL
lmm Dor.
6
cat #Q30, secs. 85 & 88
scc.
GCL ~
[~Vv'
\
--'-
~
~t
R
C lmm
• labeled cell
Fig. 1, A: The locations of the BDA injection sites in the left cochlear nuclei of 3 cats. B: Camera lucida drawing of the locations of BDA-labeled cells (solid dots) in two sections of cat #Q30. The region of the VNR examined in the present study was restricted to the portion immediately ventral to the AVCN (i.e., lateral to the dashed line in the VNR). Thick and thin line segments represent thick and thin BDA-labeled fibers. Arrows identify thick BDA-labeled fibers peripheral to the Schwann cell-glial border in the VN. Arrow head identifies the granule-cell populated corner between AVCN and VNR. C: Camera lucida drawings of BDA-labeled cells in the VNR. Arrows identify the axons. AA: anterior part of anterior division of AVCN; AP: posterior part of anterior division of AVCN; GCL: granule cell layer; PD: dorsal part of posterior division of AVCN; PV: ventral part of posterior division of AVCN; SCC: small cell cap; SGB: Schwann-cell-glial border; VN: vestibular nerve; VNR: vestibular nerve root.
cells in VNR
BDA-labeled
80
80 A
I
B
N=155
60
6O
~. 40
40 20
20
0.0
i
r
I
I
I
0.2
0.4
0.6
0.8
1.0
ol 0
50
(short diameter) / (long diameter)
100
150
cell body
100
200
area
250
450
(~tm2)
80 C
8O
D
"/
60
,~ 60 -~ 40 E ¢
2O
0
l[
40
20
i
i
i
5
l0
15
0
i
20
25
short diameter (p.m)
30
40
r
0
5
10
15
i
r
20
25
30
40
long diameter (p.m)
Fig. 2. Distribution of the ratio of short to long diameters (A), cell body area (B), short (C) and long diameters (D) of BDA-labeled cells in the cat VNR.
H.B. Zhao et al. / Brain Research 700 (1995) 295-298
Table 1 Summary of BDA injection in the CN Animal Injection site number
Q30 Q28 Q45 Q39 Q37 Q34 Q33
Depth CF No. of Amount of (/zm) (kHz) labeled labeled cells in fibers in VNR VNR
marginal AVCN 300 marginal AVCN 400 marginal AVCN 200 marginalAVCN 150 marginal AVCN 150 core AVCN 900 deep DCN 600
20 13 16 5.3 8.0 4.0 6.0
87 42 0 23 3 0 0
+ + + + + +
+++ +++ + +
Axons were visible in some labeled cells (Fig. 1C, arrows). The labeled fibers traveled along the marginal A V C N to the lateral corner between the A V C N and V N R (Fig. 1B, arrow head) and cascaded into the VNR. Some of the labeled fibers were thick (diameter > 1 /.tm; Fig. 1B) and were found in the V N R and peripheral to the Schwann cell-glial border (e.g., Fig. 1B, arrows). The trajectories of the thick fibers resemble those of the medial olivocochlear fibers in the V N R and A V C N [4,5]. Thin labeled fibers (diameter < 1 /xm) in the V N R were often varicose, with a string of swellings exceeding 1 /zm in diameter. Both thick and thin B D A - l a b e l e d fibers could be seen in the VNR, even when few or no labeled cells were found in the V N R (e.g., cat Q45 and Q37, Table 1). Quantitative measurements of a total of 155 labeled cells in the V N R are shown in Fig. 2. The distribution of the ratio of the short to long diameters of the somata of the labeled cells showed a single peak centered at 0 . 6 - 0 . 8 (Fig. 2A). The median and mean soma areas of the labeled cells were 111 and 118 /.~m2, respectively, equivalent to circular diameters of 11.9 and 12.3 /zm. The distributions of the short and long diameters are shown in Fig. 2C,D. Their means were 9.8 /zm and 15.2 /zm, respectively. The main finding of the present study is that small cells embedded in the V N R were labeled after injections of B D A into marginal shell regions of the cat AVCN. This is an unexpected new finding. Some of the labeled cells (e.g., cells 2, 7 - 1 0 , Fig. 1C) resembled the Golgi-impregnated cat CN granule cells (diameter = 1 0 - 1 1 /xm) [12]. They both are small in size and have sparsely branched dendritic trees that often arise out of thick trunks. Other labeled cells (e.g., cells 1, 3 - 6 , Fig. 1C) resembled the small cells of the V C N SCC as the latter are also often oval to spindleshaped [13]. Given the resemblance and connection, we postulate that the labeled cells in the V N R may be a part of a large system of granule cells and small cells that includes the CN and V N R besides other parts of the brain. What are possible functions of the projection of the small cells in the V N R to the A V C N marginal shell? Recently, primary vestibular afferent projections to the CN have been described [6,8]. McCue and Guinan [11] found that primary vestibular fibers from the saccule were acous-
297
tically sensitive and that one such fiber, intracellularly labeled, arborized in a region ventromedial to the CN. Also, the medial and lateral olivocochlear fibers give collateral inputs to vestibular nuclei [5]. These findings suggest that the vestibular and auditory systems may influence each other. A possible role for the small VNR neurons of the present study may be to serve as secondorder vestibular neurons that convey information from vestibular end organs to the CN. This possibility is consistent with a hypothesis that the granule c e l t s / s m a l l cells of the marginal A V C N act to integrate auditory information with that of other modalities [9]. In addition, the small V N R neurons may act as interneurons bet~veen the olivocochlear fibers and the CN. The present labeled cells in the V N R are not likely to be a part of the interstitial nucleus of the vestibular nerve (INVN). The INVN is located between the dorsomedial parts of the A V C N and the spinal trigeminal tract [2], whereas the present cells were located in an area ventral to the A V C N (Fig. 1B). The small sizes of the present VNR cells are also distinct from those of giant cells found in the INVN.
Acknowledgements This study was supported in part by grants R01DC00360 and P01DC01366 from NIDCD, NIH. W e thank Drs. E. Mugnaini, E.M. Ostapoff, D.L. Oliver, and D.K. Morest for comments, and Dr. D.K. Morest for help in determining cytoarchitectonic subdivisions of the cochlear nucleus.
References [1] Brawer J.R., Morest D.K. and Kane E.C., The neuronal architecture of the cochlear nucleus of the cat, J. Comp. NeuroL, 155 (1974) 251-299. [2] Brodal A. and Pompeiano O., The vestibular nuclei in the cat, J. Anat., 91 (1957) 438-454. [3] Brown M.C., Berglund A.M., Kiang N.Y.S. and Ryugo, D.K., Central trajectories of type II spiral ganglion neurons, J. Comp. Neurol., 278 (1988) 581-590. [4] Brown M.C., Liberman M.C., Benson T.E. and Ryugo, D.K., Brainstem branches from olivocochlear axons in cats and rodents, J. Comp. Neurol., 278 (1988) 591-603. [5] Brown M.C., Fiber pathways and branching patterns of biocytinlabeled olivocochlear neurons in the mouse brainstem, J. Comp. Neurol., 337 (1993) 600-613. [6] Burian M. and Gstoettner W., Projection of primary vestibular afferent fibers to the cochlear nucleus in the guinea pig, Neurosci. Lett., 84 (1988) 13-17. [7] Itoh K., Kamiya H., Mitani A., Yasui Y., Takada M. and Mizuno, N., Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat, Brain Res., 400 (1987)145-150. [8] Kevetter G.A. and Perachio A.A., Projections from the sacculus to the cochlear nuclei in the mongolian gerbil, Brain Behav. EL'ol., 34 (1989) 193-200. [9] Kim D.O., Zhao H., Parham K. and Ghoshal S., Projection of small
298
H.B. Zhao et al. /Brain Research 700 (1995) 295-298
neurons in the vestibular nerve root to the granule-cell-layer/smallcell-cap of the anteroventral cochlear nucleus of the cat, Assoc. Res. Otolaryngol. Abst., 18 (1995) 37. [10] Liberman M.C., Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus, J, Comp. Neurol., 313 (1991) 240-258. [11] McCue M.P. and Guinan J.J., Acoustically responsive fibers in the vestibular nerve of the cat, J. Neurosci., 14 (1994) 6058-6070. [12] Mugnaini E., Warr B.W. and Osen K.K., Distribution and light
microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse, .L Comp. NeuroL, 191 (1980) 581-606. [13] Osen K.K., Cytoarchitecture of the cochlear nuclei in the cat, J. Comp. NeuroL, 136 (1969) 453-484. [14] Weinberg R.J. and Rustioni A., A cuneocochlear pathway in the rat, Neuroscience, 20 (1987) 209-219. [15] Veenman C.L., Reiner A. and Honig M.G., Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies, J. Neurosci. Methods, 41 (1992) 239-254.
Brain Research 700 (1995) 295-298
Short communication
Small neurons in the vestibular nerve root project to the marginal shell of the anteroventral cochlear nucleus in the cat H.B. Zhao, K. Parham, S. Ghoshal, D.O. Kim * Division of Otolaryngology, Surgical Research Center, Department of Surgery and Neuroscience Program, UniL,ersity of Connecticut Health Center, Farmington, CT06030-1110, USA Accepted 16 August 1995
Abstract
We injected biotinylated dextran amine (BDA) into marginal shell regions of the anteroventral cochlear nucleus (AVCN) of the cat. These injections led to retrograde labeling of cells including small cells (median soma area = 111 /xm 2, equivalent diameter = 11.9/xm) in the vestibular nerve root (VNR), just ventral to an anterior part of the AVCN. This is an unexpected new finding. The cells were scattered among BDA-labeled fibers and were oriented parallel to the course of the VNR fibers. We suggest that the small neurons of the VNR might serve as second-order vestibular neurons conveying information from vestibular end organs to the cochlear nucleus (CN) and/or act as interneurons between the olivocochlear fibers in the VNR and the CN. Keywords: Small cell cap; Granule cells; Auditory brain stem; Biotinylated dextran amine; Retrograde transport; Olivocochlear fibers
The ventral cochlear nucleus (VCN) has a surrounding shell of granule cells and small cells [1,12,13]. A number of studies identified projections from a variety of origins to anteroventral cochlear nucleus (AVCN) marginal regions, including type II spiral ganglion cells [3], type I spiral ganglion cells physiologically characterized by low spontaneous rates [10], collaterals of the medial olivocochlear fibers [4], dorsal column nuclei [7,14] and primary vestibular afferent fibers [6,8]. Since the marginal shell of the VCN was not the focus of the above cited studies, the connections of this region remain largely unexplored. We used a complimentary approach of depositing a tracer into the region to identify sources of inputs. The left CN of the cat was exposed. The tracer-filled micropipette, 10% biotinylated dextran amine (BDA) (Molecular Probes) in 0.9% saline, was lowered into the CN. A focal injection ( < 100 nl) of the tracer was made using a Picospritzer (General Valve Co.). The cat survived for 7 - 8 days and transcardially perfused. B D A was visualized with avidin-biotin-peroxidase complex (ABC) histochemistry (Vector Laboratories) [15]. The extent of the BDA injection site was defined by the presence of extracellular BDA. Quantitative measurements of cell area and
* Corresponding author. E-maih [email protected]. 0006-8993/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved
SSD1 0 0 0 6 - 8 9 9 3 ( 9 5 ) 0 1 0 7 8 - 5
diameter were obtained using a computerized system (MicroBrightField Neurolucida). Injection of B D A into the marginal shell of the A V C N (Fig. 1A) resulted in labeling of small cells and fibers scattered throughout the body of the vestibular nerve root (VNR), just ventral to an anterior region of the A V C N and central to the Schwann cell-glial border of the vestibular nerve (VN) (Fig. 1B). Although these injections also labeled cell bodies and fibers in other parts of the brain, the present report is restricted to the VNR as outlined in Fig. lB. When the focal injection sites were primarily restricted to the granule cell layer (GCL) minimally extending into the small cell cap (SCC) (Q45, Fig. 1A; Q37, not shown), few or no labeled cells were found in the VNR (Table 1). When the injection sites included the SCC and little involved the lateral margins of the PD and PV areas of the A V C N (Q30 and Q28, Fig. 1A; Q39, not shown), there were substantially more labeled cells in the VNR (Table 1). When injection sites were placed in the A V C N core (cat Q34) or deep dorsal CN (DCN) (cat Q33), with little infringement on the marginal regions of the AVCN, no labeled cells were found in the VNR (Table 1). The cell bodies of the labeled cells in the VNR were spindle-shaped or ovoid (Fig. 1C). The dendrites of the labeled cells were usually visible, often including a few branches, and were parallel to the vestibular afferent fibers.
296
H.B. Zhao et al. / Brain Research 700 (1995) 295-298
Dot.
cat# Q30 ~ , / GCL~/~
eat# Q28
cat# Q45
i
GCL
lmm Dor.
6
cat #Q30, secs. 85 & 88
scc.
GCL ~
[~Vv'
\
--'-
~
~t
R
C lmm
• labeled cell
Fig. 1, A: The locations of the BDA injection sites in the left cochlear nuclei of 3 cats. B: Camera lucida drawing of the locations of BDA-labeled cells (solid dots) in two sections of cat #Q30. The region of the VNR examined in the present study was restricted to the portion immediately ventral to the AVCN (i.e., lateral to the dashed line in the VNR). Thick and thin line segments represent thick and thin BDA-labeled fibers. Arrows identify thick BDA-labeled fibers peripheral to the Schwann cell-glial border in the VN. Arrow head identifies the granule-cell populated corner between AVCN and VNR. C: Camera lucida drawings of BDA-labeled cells in the VNR. Arrows identify the axons. AA: anterior part of anterior division of AVCN; AP: posterior part of anterior division of AVCN; GCL: granule cell layer; PD: dorsal part of posterior division of AVCN; PV: ventral part of posterior division of AVCN; SCC: small cell cap; SGB: Schwann-cell-glial border; VN: vestibular nerve; VNR: vestibular nerve root.
cells in VNR
BDA-labeled
80
80 A
I
B
N=155
60
6O
~. 40
40 20
20
0.0
i
r
I
I
I
0.2
0.4
0.6
0.8
1.0
ol 0
50
(short diameter) / (long diameter)
100
150
cell body
100
200
area
250
450
(~tm2)
80 C
8O
D
"/
60
,~ 60 -~ 40 E ¢
2O
0
l[
40
20
i
i
i
5
l0
15
0
i
20
25
short diameter (p.m)
30
40
r
0
5
10
15
i
r
20
25
30
40
long diameter (p.m)
Fig. 2. Distribution of the ratio of short to long diameters (A), cell body area (B), short (C) and long diameters (D) of BDA-labeled cells in the cat VNR.
H.B. Zhao et al. / Brain Research 700 (1995) 295-298
Table 1 Summary of BDA injection in the CN Animal Injection site number
Q30 Q28 Q45 Q39 Q37 Q34 Q33
Depth CF No. of Amount of (/zm) (kHz) labeled labeled cells in fibers in VNR VNR
marginal AVCN 300 marginal AVCN 400 marginal AVCN 200 marginalAVCN 150 marginal AVCN 150 core AVCN 900 deep DCN 600
20 13 16 5.3 8.0 4.0 6.0
87 42 0 23 3 0 0
+ + + + + +
+++ +++ + +
Axons were visible in some labeled cells (Fig. 1C, arrows). The labeled fibers traveled along the marginal A V C N to the lateral corner between the A V C N and V N R (Fig. 1B, arrow head) and cascaded into the VNR. Some of the labeled fibers were thick (diameter > 1 /.tm; Fig. 1B) and were found in the V N R and peripheral to the Schwann cell-glial border (e.g., Fig. 1B, arrows). The trajectories of the thick fibers resemble those of the medial olivocochlear fibers in the V N R and A V C N [4,5]. Thin labeled fibers (diameter < 1 /xm) in the V N R were often varicose, with a string of swellings exceeding 1 /zm in diameter. Both thick and thin B D A - l a b e l e d fibers could be seen in the VNR, even when few or no labeled cells were found in the V N R (e.g., cat Q45 and Q37, Table 1). Quantitative measurements of a total of 155 labeled cells in the V N R are shown in Fig. 2. The distribution of the ratio of the short to long diameters of the somata of the labeled cells showed a single peak centered at 0 . 6 - 0 . 8 (Fig. 2A). The median and mean soma areas of the labeled cells were 111 and 118 /.~m2, respectively, equivalent to circular diameters of 11.9 and 12.3 /zm. The distributions of the short and long diameters are shown in Fig. 2C,D. Their means were 9.8 /zm and 15.2 /zm, respectively. The main finding of the present study is that small cells embedded in the V N R were labeled after injections of B D A into marginal shell regions of the cat AVCN. This is an unexpected new finding. Some of the labeled cells (e.g., cells 2, 7 - 1 0 , Fig. 1C) resembled the Golgi-impregnated cat CN granule cells (diameter = 1 0 - 1 1 /xm) [12]. They both are small in size and have sparsely branched dendritic trees that often arise out of thick trunks. Other labeled cells (e.g., cells 1, 3 - 6 , Fig. 1C) resembled the small cells of the V C N SCC as the latter are also often oval to spindleshaped [13]. Given the resemblance and connection, we postulate that the labeled cells in the V N R may be a part of a large system of granule cells and small cells that includes the CN and V N R besides other parts of the brain. What are possible functions of the projection of the small cells in the V N R to the A V C N marginal shell? Recently, primary vestibular afferent projections to the CN have been described [6,8]. McCue and Guinan [11] found that primary vestibular fibers from the saccule were acous-
297
tically sensitive and that one such fiber, intracellularly labeled, arborized in a region ventromedial to the CN. Also, the medial and lateral olivocochlear fibers give collateral inputs to vestibular nuclei [5]. These findings suggest that the vestibular and auditory systems may influence each other. A possible role for the small VNR neurons of the present study may be to serve as secondorder vestibular neurons that convey information from vestibular end organs to the CN. This possibility is consistent with a hypothesis that the granule c e l t s / s m a l l cells of the marginal A V C N act to integrate auditory information with that of other modalities [9]. In addition, the small V N R neurons may act as interneurons bet~veen the olivocochlear fibers and the CN. The present labeled cells in the V N R are not likely to be a part of the interstitial nucleus of the vestibular nerve (INVN). The INVN is located between the dorsomedial parts of the A V C N and the spinal trigeminal tract [2], whereas the present cells were located in an area ventral to the A V C N (Fig. 1B). The small sizes of the present VNR cells are also distinct from those of giant cells found in the INVN.
Acknowledgements This study was supported in part by grants R01DC00360 and P01DC01366 from NIDCD, NIH. W e thank Drs. E. Mugnaini, E.M. Ostapoff, D.L. Oliver, and D.K. Morest for comments, and Dr. D.K. Morest for help in determining cytoarchitectonic subdivisions of the cochlear nucleus.
References [1] Brawer J.R., Morest D.K. and Kane E.C., The neuronal architecture of the cochlear nucleus of the cat, J. Comp. NeuroL, 155 (1974) 251-299. [2] Brodal A. and Pompeiano O., The vestibular nuclei in the cat, J. Anat., 91 (1957) 438-454. [3] Brown M.C., Berglund A.M., Kiang N.Y.S. and Ryugo, D.K., Central trajectories of type II spiral ganglion neurons, J. Comp. Neurol., 278 (1988) 581-590. [4] Brown M.C., Liberman M.C., Benson T.E. and Ryugo, D.K., Brainstem branches from olivocochlear axons in cats and rodents, J. Comp. Neurol., 278 (1988) 591-603. [5] Brown M.C., Fiber pathways and branching patterns of biocytinlabeled olivocochlear neurons in the mouse brainstem, J. Comp. Neurol., 337 (1993) 600-613. [6] Burian M. and Gstoettner W., Projection of primary vestibular afferent fibers to the cochlear nucleus in the guinea pig, Neurosci. Lett., 84 (1988) 13-17. [7] Itoh K., Kamiya H., Mitani A., Yasui Y., Takada M. and Mizuno, N., Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat, Brain Res., 400 (1987)145-150. [8] Kevetter G.A. and Perachio A.A., Projections from the sacculus to the cochlear nuclei in the mongolian gerbil, Brain Behav. EL'ol., 34 (1989) 193-200. [9] Kim D.O., Zhao H., Parham K. and Ghoshal S., Projection of small
298
H.B. Zhao et al. /Brain Research 700 (1995) 295-298
neurons in the vestibular nerve root to the granule-cell-layer/smallcell-cap of the anteroventral cochlear nucleus of the cat, Assoc. Res. Otolaryngol. Abst., 18 (1995) 37. [10] Liberman M.C., Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus, J, Comp. Neurol., 313 (1991) 240-258. [11] McCue M.P. and Guinan J.J., Acoustically responsive fibers in the vestibular nerve of the cat, J. Neurosci., 14 (1994) 6058-6070. [12] Mugnaini E., Warr B.W. and Osen K.K., Distribution and light
microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse, .L Comp. NeuroL, 191 (1980) 581-606. [13] Osen K.K., Cytoarchitecture of the cochlear nuclei in the cat, J. Comp. NeuroL, 136 (1969) 453-484. [14] Weinberg R.J. and Rustioni A., A cuneocochlear pathway in the rat, Neuroscience, 20 (1987) 209-219. [15] Veenman C.L., Reiner A. and Honig M.G., Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies, J. Neurosci. Methods, 41 (1992) 239-254.