THE JOURNAL OF COMPARATIVE NEUROLOGY 314~306-318 (1991)

Central Projections of Auditory Nerve

Fibers in the Barn Owl
C.E. CARR AND R.E. BOUDREAU
Department of Neurobiology and Anatomy, University of Rochester, Rochester,
New York 14642

ABSTRACT
The central projections of the auditory nerve were examined in the barn owl. Each auditory
nerve fiber enters the brain and divides to terminate in both the cochlear nucleus angularis and
the cochlear nucleus magnocellularis. This division parallels a functional division into intensity
and time coding in the auditory system. The lateral branch of the auditory nerve innervates the
nucleus angularis and gives rise to a major and a minor terminal field. The terminals range in
size and shape from small boutons to large irregular boutons with thorn-like appendages. The
medial branch of the auditory nerve conveys phase information to the cells of the nucleus
magnocellularis via large axosomatic endings or end bulbs of Held. Each medial branch divides
to form 3-6 end bulbs along the rostrocaudal orientation of a single tonotopic band, and each
magnocellular neuron receives 1-4 end bulbs. The end bulb envelops the postsynaptic cell body
and forms large numbers of synapses. The auditory nerve profiles contain round clear vesicles
and form punctate asymmetric synapses on both somatic spines and the cell body.

Key words: time, intensity, phase, end bulbs, magnocellularis,angularis

The external ears of barn owls are oriented asymmetri-
cally in the vertical plane (Norberg, '78). Because of this
asymmetry, interaural intensity differences vary more with
the elevation of the sound source than with azimuth. Barn
owls are therefore able to use interaural intensity differ-
ences to localize sounds in elevation, while using interaural
time differences to determine the azimuthal location of a
sound (Konishi, '73b; Olsen et al., '89; Moiseff, '89). These
binaural cues are processed in separate time and intensity
pathways that begin with the auditory nerve projections to
the two cochlear nuclei (Sullivan and Konishi, '84; Taka-
hashi et al., '84; Takahashi and Konishi, '88; Konishi et al.,
'88). Time and intensity information is recombined a t the
level of the auditory midbrain to form a two-dimensional
map of auditory space (Knudsen and Konishi, '78; Knud-
sen, '80; Takahashi et al., '84; Wagner et al., '87).
The auditory nerve enters the brain and divides to
innervate the two cochlear nuclei. The cochlear nucleus
angularis contains neurons that are more sensitive to
changes in sound level, while the firing patterns in the
cochlear nucleus magnocellularis preserve the phase infor-
mation encoded in the auditory nerve (Sullivan and Kon-
ishi, '84; Sullivan, '85; Konishi et al., '85). This functional
division into intensity and time coding begins with the
morphology of the auditory nerve projections to the co-
chlear nuclei, The branch of the auditory nerve that
terminates in the nucleus angularis forms small terminal
boutons, while the branches to the nucleus magnocellularis
terminate as end bulbs of Held (Konishi et al., '88).
The projections of single auditory nerve fibers to the time
and intensity coding cochlear nuclei will be described in this
paper. Morphologically distinct auditory nerve terminals
characterize the different cochlear nuclei in all reptiles,
birds and mammals (Boord and Rasmussen, '63; Boord, '68;
Rube1 and Parks, '75; Jhaveri and Morest, '82b; Miller, '85;
Browner and Marbey, '88; Spzir et al., '90; Carr, '91). In the
barn owl, these distinctions underlie the parallel processing
of time and intensity information in the auditory system.
Since the separation of time and intensity pathways is
highly developed in the owl, those features specialized for
phase-locking or preservation of sound intensity informa-
tion may be more obvious in owls than in other animals.
MATERIALS AND METHODS
These results are based on studies of 11 adult barn owls
(Tyto alba) of both sexes. All owls were also used in parallel
studies (Takahashi et al., '87; Carr and Konishi, '88; Fujita
and Konishi, '90; Carr and Konishi, '90). Details regarding
stereotaxis, surgery, and acoustic stimulation are available
elsewhere (Takahashi and Konishi, '88; Carr and Konishi,
'90).
Anatomy
Horseradish peroxidase (HRP) was used as a tracer to
study the projections of the auditory nerve in six owls.
Accepted September 7,1991.

o 1991 WILEY-LISS. INC.


OWL AUDITORY NERVE
I ROSTRAL
Fig. 1. Projections of the auditory nerve to the cochlear nucleus
magnocellularis (NM) and the cochlear nucleus angularis (NA).Camera
lucida reconstruction of two auditory nerve fibers (8N) imposed upon
two drawings of transverse sections through the brainstem, one (mostly
hidden) at the level of the eighth nerve entry, and the other through the
central region of the nucleus magnocellularis. Upon entering the brain,
the root branch of each auditory nerve fiber divides to form a lateral
branch to the nucleus angularis (only one arbor is shown within the
nucleus angularis) and a medial branch to the 7 kHz region of the
nucleus magnocellularis. The medial branches above the nucleus
magnocellularis give rise to 3 4 collaterals, each tipped by an end bulb.
The lateral branch is thinner than the auditory nerve, being 1.7 km
Injections were made into regions of the auditory nerve and
into the nucleus magnocellularis. Birds were anesthetized
by intramuscular injection of ketamine hydrochloride (33
mglkglhour, Vetalar, Bristol laboratories), and the skull
immobilized. After a craniotomy, the structure of interest
in the auditory brainstem was stereotaxically and physiolog-
ically identified. Extracellular injections of HRP were then
carried out with a glass pipette of 20-40 pm diameter. HRP
(Boeringer-Mannheim) was prepared in filtered 0.5M KC1-
Tris buffer at pH 7.6, and iontophoresed with 2 FA pulsed
positive current for 5-10 minutes. Sufficient neural activity
was recorded through these electrodes to identify the best
frequency at the recording site. After the injection, the
craniotomy was sealed with dental cement and the scalp
was sutured. Antibiotic cream and additional local anes-
thetic were applied to the wound and the owl returned to its
home cage. Twenty-four hours to 3 days later, the owls were
anesthetized with ketamine as before, followed by a lethal
dose of nembutal (100 mg/kg IM; Abbott laboratories).
After intracardiac injection of heparin, owls were perfused
transcardially with normal saline, followed immediately by
1 liter of 1.25% glutaraldehyde, 2% paraformaldehyde in
0.1M phosphate buffer at pH 7.2. The brain was postfixed
overnight a t 4"C, sectioned at 100 pm in cold phosphate
307
diameter (?0.4,n = 29) a s opposed to 3 pm (t-0.4, n = 16). The medial
branch to the nucleus magnocellularis is similar in diameter to the root
branch (mean = 3.1 Fm, 5 0 . 7 , n = 16). Note that this reconstruction
has been highly compressed in the rostrocaudal dimension, and that the
nucleus magnocellularis becomes much larger than shown in caudal
sections. NL = nucleus laminaris. Bar = 1 mm. Inset: Schematic
horizontal view of the nucleus magnocellularis showing the path taken
by a labeled auditory nerve axon with a best frequency of 5.5 kHz. The
most lateral collateral into the nucleus magnocellularis in this figure is
the most caudal. Additional branches are given off at intervals as the
fiber travels rostromedial.
buffer on a vibratome, and then sections were processed
with diaminobenzidine as a chromagen (Adams, '81). The
best-labelled fibers were reconstructed with the aid of a
camera lucida according to the method of Sereno and
Ulinski ('87), as previously described (Carr and Konishi,
'88). No correction was made for tissue shrinkage.
The rapid Golgi technique (Valverde, '70) was used on
three owls. They were anesthetized with ketamine, followed
by a lethal dose of nembutal (100 mgikg IM; Abbott
laboratories). After intracardiac injection of heparin, owls
were perfused transcardially with normal saline, followed
immediately by 1 liter of 4% paraformaldehyde in 0.1M
phosphate buffer at pH 7.2. The brain was postfixed
overnight, then blocked transversely and placed in Golgi
fixative. End bulbs were found in two of three brains.
Electron microscopy
For normal ultrastructural studies, two owls were anes-
thetized as above and perfused transcardially with avian
Tyrode's solution (Jackson and Parks, '821, followed by 1
liter of 3% glutaraldehyde, 1%paraformaldehyde in 0.1 M
phosphate buffer at pH 7.4. The brain was postfixed
overnight, then sectioned on a vibratome. Selected regions
308
were postfixed with 1.0% osmium tetroxide. Following
postfixation, the tissue was dehydrated and embedded in
Polybed 812 resin. Thin sections were stained with uranyl
acetate and Reynold's lead stain, and examined with a Zeiss
electron microscope.
RESULTS
After the auditory nerve enters the brain, it divides into a
medial and a lateral branch. The thinner lateral branch
exits the auditory nerve root, and travels dorsally and
rostrally to terminate within the nucleus angularis. The
thicker medial branch runs above the nucleus magnocellu-
laris, giving off collaterals which terminate as end bulbs on
the cell body of the magnocellular neurons (Fig. 1).No
branches were seen in the auditory nerve before the
schwann-glialborder.
The nucleus angularis may be tonotopically
organized
The lateral ascending branch of the auditory nerve
terminates in the nucleus angularis. The topography of this
- '. - _ - - - - - - - - _ _ _ _ _-
_ -- - '
I
' II
Fig. 2. Projection of the lateral branch of the auditory nerve to the
nucleus angularis shown in camera lucida reconstructions. Bar = 200
pm. A: Auditory nerve branch labeled after a small HRP injection into
the 7 kHz region of the nucleus magnocellularis (same as shown in Fig.
1). C marks the caudal terminal field and R the thicker rostra1
projection. B: Auditory nerve branch in the nucleus angularis after
C.E. CARR AND R.E. BOUDREAU
projection to the nucleus angularis is complex. The nucleus
angularis has been described as an inverted U-shaped cell
group on the dorsolateral aspect of the eighth nerve root
(Takahashi and Konishi, '88). The lateral branch of the
auditory nerve travels along the medial edge of the nucleus,
and gives off a collateral to the medial arm of this U. The
branch may enter the nucleus angularis through the center
of the U, or at any point along the medial border of the U.
The eventual termination site appears to be dependent on
the best frequency of the fiber, since physiological studies
have suggested that the nucleus angularis is tonotopically
organized (Sullivan, '85). Small injections of HRP into the
nucleus magnocellularis and the auditory nerve were used
to determine the tonotopic order of the projection to the
nucleus angularis. Injections into low best-frequency re-
gions labelled auditory nerve fibers in the ventromedial arm
of the U, while injections into higher-frequency regions
labelled more dorsal regions of the nucleus angularis (Fig. 2
inset). Single fiber labelling combined with the location on
the basilar papilla of the auditory nerve terminals may be
required, however, for unequivocal identification of tono-
topic order in the nucleus angularis.
<--
I'
HRP injection into the 5.5 kHz region of the nucleus magnocellularis.
Inset: Locations of the terminal fields in the nucleus angularis after
injections into the 5, 6, and 7 kHz regions of the nucleus magnocellu-
laris. With this proposed tonotopic order in the nucleus angularis, high
best-frequency projections are found dorsal to lower best-frequency
projections.
OWL AUDITORY NERVE
Two terminal fields in the nucleus angularis
Interpretation of the tonotopic order in the nucleus
angularis is complicated because reconstructions of 16
HRP-labeled auditory nerve fibers showed that the lateral
branch forms two terminal fields within the nucleus (Fig.
2 ) . The lateral branch enters the nucleus angularis and
gives off one or more thin collaterals, collectively called the
minor branch. These thin collaterals form a small terminal
field near the site of entry of the lateral branch. The major
branch travels rostrally to terminate in more dorsal and
lateral regions of the nucleus (Fig. 2). The major and minor
terminal fields are generally not contiguous.
The endings in the nucleus angularis exhibited a wide
variety of shapes and sizes (Fig. 3). The minor branch or
thin collaterals formed both complex and simple bouton
endings and en passant swellings. Terminals were found
both in the neuropil and surrounding cell bodies. The thin
collaterals also sometimes terminated in fine blunt endings
(Fig. 3, arrows), called free terminals after Rouiller et al.
('86). One unusual type of thin collateral ending is shown in
Figure 3, upper left. This complex ending ended in a fine
brush of terminals that did not make axosomatic contact,
but ended in the neuropil. The major branch generally
divided into two or three thick collaterals. The thick
collaterals usually ended in complex thorn-like swellings,
although simple boutons and en passant swellings were also
found.
Fig. 3. Camera lucida drawing of selected auditory nerve collaterals
from transverse sections through the nucleus angularis. Dotted lines
indicate the cell body of angularis neurons. Bar = 40 Fm. Left: Both
simple bouton endings, en passant swellings, and small complex
309
Each auditory nerve axon forms several end
bulbs in the nucleus magnocellularis
The medial branch of each auditory nerve fiber inner-
vates the cochlear nucleus magnocellularis and gives rise to
the large axosomatic endings termed end bulbs of Held (Fig.
4).These medial branch s o n s travel on the dorsal surface
of the brainstem, above the nucleus magnocellularis (Fig.
1). Each axon gives off 3-6 branches along its caudal to
rostral traverse, and each branch terminates in a single end
bulb. The distribution of these individual branches corre-
sponds to the tonotopic organization of the nucleus (Taka-
hashi and Konishi, '88; Carr and Konishi, '90).Usually the
main nerve trunk above the nucleus magnocellularis gives
off a single collateral at a time, but three- or four-part
divisions were also observed. Once each collateral leaves the
main trunk, it travels ventrally into the nucleus magnocel-
lularis to form a single end bulb on a magnocellular cell
body (Figs. 4,5).
In some heavily labeled HRP material, the terminal
portions of auditory nerve axons in the nucleus magnocellu-
laris form swellings at the nodes of Ranvier (Fig. 4). These
swellings have also been identified as nodes of Ranvier in
HRP-labelled auditory nerve fibers in the cat (Fekete et al.,
'82). The swellings enabled nodes to be recognized at the
level of the light microscope. Internodal distances decreased
in the last three nodes before the end bulb (Fig. 4B, inset).
Similar measurements were obtained at the ultrastructural
endings (arrows) arise from these two thin collaterals in the caudal
terminal field. Right: Complex thorn-like swellings predominate in the
rostral terminal field in the nucleus angularis.
310
Fig. 4. Variation in size and percentage cover of magnocellular
neurons is illustrated in these camera lucida reconstructions of HRP-
labelled end bulbs. The two end bulbs on the left envelop their target
cells. Each cell appears to receive only one end bulb. The center left end
bulb is also shown in Figure 5A. The two end bulbs on the right each
occupy about a third of the area of the postsynaptic cell (shown in
outline on far right). These cells appear to receive more than one end
level. End bulbs are generally myelinated to within 10 km
of the point where they enveloped the postsynaptic cell (Fig.
7A). This is true for both high and low best-frequency
regions of the nucleus, but not for the cytologically distinct
lagenar region of the nucleus magnocellularis (Takahashi
and Konishi, '88). The lagena nerve axons have an entirely
distinct morphology that will not covered in this paper.
Each end bulb forms a net of fibers that envelops a
magnocellular neuron. This synapse creates a powerful
synaptic drive, allowing for the preservation of phase-
locked responses to the auditory stimulus. End bulbs vary
in size and shape (Figs. 4,5 ) . All endings wrap around the
cell body of the postsynaptic cell, but most do not occupy the
entire area of the cell body (Fig. 4,right hand side). When
each auditory nerve axon reaches its target cell body, the
main trunk of the end bulb gives off several thick branches
and continues down the long axis of the magnocellular cell
body, giving off smaller branches. These branches are
irregular in shape, and the spaces between them are filled
by smaller processes. Rarely, fine collaterals leave the end
bulb and form varicose processes (Fig. 4, right). These
collaterals are short (20-50 km) and appear to contact
neighboring neurons.
Magnocellular neurons receive more than one
end bulb
When many auditory nerve fibers were labelled after a
large HRP injection into the auditory nerve, it could be
C.E. CARR AND R.E. BOUDREAU
bulb. Regular swellings on the preterminal axon (arrows)mark nodes of
Ranvier. Bar = 30 Fm. Inset: Interodal distances increase with
distance from the terminal. The mean distance between t h e last node
and the end bulb was 47 pm (S.D. = 210, n = 141, then 54 (18,n = 91,
then 65 (211, n = 5 ) . Internodes at a distance from the terminal are
greater than 150 pm apart.
observed that most magnocellular neurons received more
than one labelled end bulb (Fig. 5 ) . Each end bulb occupied
separate non-overlapping domains on the cell body surface.
Since ultrastructural observations have shown that audi-
tory nerve terminals were distributed over the entire
surface of the magnocellular neuron (Carr and Boudreau,
'881, the amount of each cell covered by a single labelled end
bulb enabled us to estimate how many cells received input
from more than one auditory nerve fiber. Counts of 189
cells using Nomarski optics showed the cell body covered by
a single labelled end bulb in 33 cases, and by more than one
end bulb in 156 cases. Thus, about 17% of all magnocellular
neurons received input from only one auditory nerve fiber,
and most received input from two or more auditory nerve
fibers. It was difficult to determine what proportion of
magnocellular neurons received more than 2 end bulbs, but
some were observed to receive three or four end bulbs (Fig.
5B).
Magnocellular neurons receive many auditory
nerve synapses
Auditory nerve synapses were usually found on magnocel-
lular cell bodies (Figs. 6-43),although they were also found
on the proximal dendrites of magnocellular neurons in the
caudal, low best-frequency region of the nucleus magnocel-
lularis (Fig. 7B). No synapses were observed on dendrites
from the high best-frequency regions of the nucleus, but no
dendrites were serially sectioned in their entirety, so we
OWL AUDITORY NERVE
Fig. 5. Photomicrographs of HRP-labelled end bulbs. Bar = 10 pm.
A This large labelled end bulb envelops the postsynaptic cell and may
be its only end bulb input. The parent axon gives off several thick
branches and wraps around the postsynaptic cell to terminate on the
opposite pole, givingoff smaller branchlets as it goes. Note the irregular
processes that originate from the thick branches. B: Three end bulbs
synapse on a single magnocellular neuron. Arrows mark each end bulb
axon. Nomarski optics show that these end bulbs do not interdigitate,
but occupy separate territories on the cell.
cannot rule out the possibility that these dendrites might
also receive a small number of synapses.
Auditory nerve synapses are small, being about 300 nm
in diameter, and they are very numerous. The total number
of auditory nerve synapses per cross section of a magnocel-
lular neuron was counted in thin sections. We found about
34 synapses per section (mean = 33.8, SD = 7.4, n = 17).
Assuming a random distribution of synapses, and a soma
area of 700 pm2 (Takahashi and Konishi, '881, we estimate
that each magnocellular neuron receives about 800 syn-
apses. Larger end bulbs make more synapses than smaller
end bulbs because large end bulbs are apposed to a larger
area of the cell.
End bulb ultrastructure
The end bulbs form large flattened terminals that en-
velop the magnocellular cell body. These terminals are
surrounded by astrocytic wrappings that may form many
layers of double membrane around the terminal (Fig. 6).
Occasionally a small glial cell process may appear as a
membrane-bound finger of cytoplasm between the end bulb
and the postsynaptic cell (Fig. 8B). In thin sections, the end
bulb terminals vary in size depending upon the plane of
311
section and their distance from the axonal end of the
terminal. Some terminals may cover most of the cell
surface, while others form large (2-5 pm) profiles that
represent sections through the irregularly shaped branches
of the end bulbs. Even small end bulb profiles may be
identified by characteristic assemblies of organelles. End
bulbs contain large numbers of small mitochondria, vesi-
cles, and membrane-bound cisterns (see below). Microtu-
bules are most commonly found at the axonal end of the
terminal.
Synapse morphology
Each end bulb forms numerous chemical synapses. These
synapses are usually on the fine (0.2-1 pm diameter)
somatic spines that indent into the end bulb. A smaller
number of synapses are located on the cell body (Fig. 8). In
counts of synapse distribution on magnocellular neurons in
the midpoint of the nucleus magnocellularis, 64% of the
auditory nerve synapses were located on the spines
(SD = L 13%, n = 19 neurons). Spine synapses may occur
on the tip or side of a somatic spine. In some planes of
section, spines may appear as circular profiles embedded in
the terminal, disconnected from their parent cell body.
These spines are filled with pale cytoplasm and limited by a
double membrane (Fig. 8). They often contain a prominent
postsynaptic density (see below).
End bulb synapses are asymmetric, with a prominent
dense undercoating on the cytoplasmic face of the magnocel-
lular neuron (Fig. 8). The synaptic cleft is about 30 nm in
width. It contains both flocculent material and fine fila-
ments that bridge the synaptic cleft. On the presynaptic
side there are usually a small cluster of 45 nm clear vesicles.
Other vesicles of the same size are distributed throughout
the cytoplasm of the end bulb. The terminals contain a
large number of membranous cisterns of varying sizes, in
addition to clathrin-coated endocytotic vesicles (Fig. 8).The
membranous cisterns are often found on either side of the
cluster of presynaptic vesicles, and may sometimes appear
fused with the presynaptic membrane (Fig. 8A). In addition
to the asymmetricjunctions associated with syapses, small
(100 nm) symmetric membrane densities or puncta ad-
haerens are often found between the terminal and the
postsynaptic cell (Fig. 8A,C).
DISCUSSION
Time and intensity cues are processed in separate time
and intensity pathways that begin with the auditory nerve
projections to the two cochlear nuclei (Sullivan and Kon-
ishi, '84; Takahashi et al., '84; Takahashi and Konishi, '88).
We have described the projections of the auditory nerve to
each cochlear nucleus. In the cochlear nucleus magnocellu-
laris, each fiber forms many end bulbs of Held. These
converging auditory nerve inputs may allow for precise
temporal coding of the phase of the auditory stimulus. In
the nucleus angularis, auditory nerve fibers form a complex
terminal field with many boutons.
Specializations for encoding of intensity
The auditory nerve terminations in the nucleus angularis
are more complex and more varied than those of the end
bulb terminations in the nucleus magnocellularis. Each
fiber has both a minor and a major terminal field. The
significance of the two terminal fields is as yet unknown.
Physiological studies have shown a simple tonotopic order
312 C.E. CARR AND R.E. BOUDREAU

Fig. 6. End bulb synapse (E) on a magnocellular neuron. Note the on either side of the end bulb are also surrounded by numerous end
many circular profiles embedded in the end bulb processes (arrow- bulb terminals. Fine astrocytic processes surround the end bulb. Bar =
heads). These are auditory nerve synapses on the somatic spines of the 5 pm.
magnocellular neuron (also see Fig. 8). The two magnocellular neurons
OWL AUDITORY NERVE
Fig. 7. End bulb synapses from high and low best-frequency regions
of the nucleus magnocellularis. A End bulbs are generally myelinated
(arrow) close to where they envelop the postsynaptic cell. This end bulb
(El is from a high best-frequency region of the nucleus magnocellularis
(MI. The terminal axon breaks up into thick branches as it reaches the
postsynaptic cell. Note the many circular profiles in the end bulb
processes where synapses are formed on the somatic spines (arrow-
heads). Also note the node (N) and astrocytic wrappings in the adjacent
313
axon, and the initial segment of a magnocellular neuron at top right
(Ax). A non-auditory nerve terminal synapses on a magnocellular
neuron (short filled arrow). Bar = 5 pm. B: Magnocellular neuron ( M i
in the low best-frequency region receive synapses on their proximal
dendrites (right) and also appear to receive more synapses on the cell
body (arrowheads) than on somatic spines. These cells also appear to
receive fewer synapses per cell cross-section than do neurons from
higher best-frequency regions. Bar = 5 pm.
314
Fig. 8. Auditory nerve synapses. A Synapses are usually found on
the fine cytoplasmic spines that indent into the end bulb. In this
transversly sectioned spine, 2-3 presynaptic dense projections may be
clearly seen at the active zone (long arrows). The postsynaptic density is
thick and sharply curved, with fibrils radiating down into the spine
neck. Indirect evidence for membrane recycling may be seen in the
presynaptic membranous cisterns located on either side of the spine
neck (short arrows) and in the many coated vesicles (arrowheads). This
terminal is also enveloped in many lamellae of glial cell membranes (*)
and attached to the postsynaptic cell by a small puncta adhaerens
(broad arrow). Bar = 0.5 Fm for both A and B. B: A variety of auditory
nerve synapses on a magnocellular neuron. The large open arrow marks
C.E. CARR AND R.E. BOUDREAU
a small cluster of vesicles localized on the presynaptic side of the
synapse. Also note the circular profiles (*) of spines cut in cross section.
Fine fibrils spanning the synaptic cleft are clearly visible. The presynap-
tic membrane contains many membranous cisterns and coated vesicles
(arrowheads).C: Synapses found on the cell body are similar to those on
spines. These two synapses both show a cluster of vesicles (large open
arrows) and presynaptic dense projections. The presynaptic terminal
contains a number of coatedvesicles (arrowheads). Note the multivesic-
ular body in the postsynaptic cell (small open arrow) and the puncta
adhaerens (large filled arrow). A presynaptic profile (*) is cut in
cross-section. Bar = 0.5 Fm.
OWL AUDITORY NERVE
in the nucleus angularis resembles that obtained from the
reconstruction of HRP-labeled auditory nerve fibers in this
paper (Konishi, '73a; Sullivan, '85). It is unlikely that the
previous electrophysiological studies could have detected
the small discontinuites introduced by the two terminal
fields. Fine grain mapping of tonotopic order within the
nucleus angularis could show whether or not the minor
terminal field serves a different function to the major field.
The diversity of endings in the nucleus angularis may
reflect the diversity of cell types in the nucleus. The nucleus
angularis contains a number of different cell types, as
judged from both cytological and immunohistochemical
criteria (Takahashi and Konishi, '88; Hausler and Sullivan,
unpublished observations). The nucleus angularis also con-
tains both GABAergic neurons and terminals (Carr et al.,
'89). Physiological studies have identified at least two cell
types in the nucleus angularis. Most neurons display "tran-
sient chopper" patterns, with a smaller number of "onset"
type units (Sullivan, '85). The role of these different cell
types in the encoding of sound intensity is as yet unknown.
The diversity of auditory nerve projections, cell types, and
physiological response types may mean that the nucleus
angularis does more than encode sound intensity, or that
the mechanism underlying encoding of intensity may re-
quire local circuit interactions.
The majority of auditory nerve terminals in both termi-
nal fields are located in the neuropil. These terminals
encode the auditory stimulus by firing in a "primary-like"
pattern, while their postsynaptic targets in the nucleus
angularis fire in regular "chopper" or "onset" patterns
(Sullivan, '85). Furthermore, auditory nerve fibers phase-
lock to the auditory stimulus, while their postsynaptic
targets in the nucleus angularis do not (Sullivan and
Konishi, '84; Sullivan, '85). The conversion from one
response type to another, and the loss of phase-locking, may
be accomplished by a number of pre- and postsynaptic
mechanisms. Presynaptic mechanisms include the follow-
ing: First, the distribution of the auditory nerve terminals
over the dendritic arbors of angularis neurons may produce
a more sustained depolarization than that observed in the
nucleus magnocellularis. Second, the lateral branch of the
auditory nerve is always smaller in diameter than the main
trunk. The reduced axon diameters and the convoluted
paths taken by auditory nerve fibers within the nucleus
angularis may act to smear the temporal precision of the
inputs. Influential postsynaptic properties could include
cell shape, electrical properties, and the distribution and
type of neurotransmitter receptors. Further experiments
could determine the different roles of these pre- and
postsynaptic modifications in intensity coding.
Specializations for encoding of phase
Both the auditory nerve and the neurons of the nucleus
magnocellularis phase-lock to auditory stimuli (Sachs and
Sinnott, '78; Sullivan and Konishi, '84; Carr and Konishi,
'90). Phase-locking is conspicuous in the barn owl. Auditory
nerve fibers show phase-locking to acoustic stimuli up to 9
kHz (Sullivan and Konishi, '841, as opposed to about 4 kHz
in the starling (Gleich and Narins, '881, 5-6 kHz in the
blackbird (Woolf and Sachs, '77; Sachs and Sinnott, '78),
and about 5-6 kHz in the cat (Johnson, '80). The barn owl
also has exceptional high-frequency hearing for a bird, with
characteristic frequencies of 9-10 kHz in the auditory
nerve (Konishi, '73b). The basilar papilla is the longest
described in birds, being about 11 mm in length (Manley
315
and Gleich, '91). The papilla is also specialized, with the
greatest specializations are found in the basal, high-
frequency portion and its overlying tectorial membrane
(Smith et al., '85; Fischer et al., '88).
Phase-locked responses are generated at the level of the
hair cell and conveyed to the auditory nerve in a way that is
not well understood. A number of morphological specializa-
tions have been correlated with phase-locking (Carr, '86).
Physiological studies have shown that the phase-locked
information that reaches the brain is preserved and may
even be improved in the nucleus magnocellularis (Sullivan
and Konishi, '84). The end bulb, with its multiple sites of
synaptic contact on the soma, provides the substrate for the
preservation of the relationship between the discharge of
the auditory nerve fibers and the neurons of the nucleus
magnocellularis. Estimates from this paper of about 800
auditory nerve synapses per magnocellular neuron indicate
that each presynaptic spike should be associated with the
injection of a large amount of current to form a large
postsynaptic potential in the magnocellular neuron.
Converging end bulb inputs may allow for an improve-
ment in phase-locking, and may explain the small increase
in vector strength observed between the auditory nerve and
the nucleus magnocellularis (Sullivan and Konishi, '84). In
the electroreceptive system of weakly electric fish, converg-
ing phase-locked inputs serve to reduce the jitter in the
timing of neuronal events, provided that the inputs possess
identical timing (Carr et al., '86). The nucleus magnocellu-
lark should therefore not just be considered a relay to the
nucleus laminaris, but also the site of further processing of
the auditory signal to improve phase-locking. The GABAer-
gic terminals that surround each magnocellular neuron
may also modulate responses to auditory stimuli (Carr et
al., '89).
Comparison with other birds
In the owl, the nucleus magnocellularis initiates a neural
pathway that encodes timing information, while the nu-
cleus angularis encodes intensity information (Sullivan and
Konishi, '84; Sullivan, '85). This parallel processing of time
and intensity information has also been proposed for the
chick (Warchol and Dallos, '90). The similarities between
the owl and chick suggests that the functional separation of
time and intensity may be a common feature of the bird
auditory system.
The general organization of the auditory nerve projec-
tions in the barn owl resembles that of other birds, al-
though the central projections of single auditory nerve
fibers have not been described in detail in other birds
(Boord and Rasmussen, '63; Whitehead and Morest, '81;
Jhaveri and Morest, '82b,c). In both barn owls and chick-
ens, the auditory nerve forms end bulb terminals in the
nucleus magnocellularis and bouton terminals in the nu-
cleus angularis (Boord and Rasmussen, '63; Whitehead and
Morest, '81). Fiber diameters are also larger in the medial
magnocellular branch than in the lateral branch to the
nucleus angularis (Whitehead and Morest, '81). In the
chicken, Whitehead and Morest ('81)found both the conven-
tional thick as well as thin fibers in the auditory nerve.
Although similar thin fibers were observed in the barn owl,
they could not be reconstructed with sufficient detail to
determine their origins or targets.
Golgi and ultrastructural studies of the auditory nerve
and the nucleus magnocellularis of the chick allow compar-
isons of end bulb morphology with the barn owl (Parks, '81;
316
Jhaveri and Morest, '82a-c). At the level of the light
microscope, end bulbs in the hatchling chick are less highly
branched and lack the fenestrated reticulum that character-
izes end bulbs in the both the barn owl and the cat (Ryugo
and Fekete, '82). These differences may either be species
differences or may be explained by the age of the chicks used
in these studies. Ryugo and Fekete ('82) have shown in the
cat that end bulbs acquire more branches with maturity,
and similar developmental changes have also been observed
in the barn owl (unpublished observations). At the ultra-
structural level, the auditory nerve synapses in the chick
are indistinguishable from those in the barn owl, except
that dense core vesicles were not seen in the barn owl
(Parks, '81).
Comparisons with reptiles
In all reptiles, including turtles, lizards, and crocodiles,
the auditory nerve fibers enter the brain and divide to
innervate two cochlear nuclei. The universality of this basic
pattern suggests that functional separation of time and
intensity information may be a common feature of the
auditory system. There is, however, a major exception to
this pattern in the lizards. Like other amniotes, lizards
have conventional auditory hair cells, the unidirectional or
tectorial population. Lizards also have uniquely derived
hair cells, termed the bidirectional or free-standing popula-
tion (Wever, '78; Miller, '80). In the alligator lizard, audi-
tory nerve fibers innervated by the unidirectional hair cell
population conform to the amniote pattern and form end
bulbs in the cochlear nucleus magnocellularis and bouton-
like terminals in the lateral nucleus angularis (Spzir et al.,
'90). Auditory nerve fibers from the bidirectional popula-
tion, however, form a unique projection to a new cochlear
nucleus, the medial nucleus angularis (Spzir et al., '90).
In the alligator lizard and bobtail lizard, the auditory
nerve fibers from the unidirectional population phase-lock
to low frequency auditory stimuli (Rose and Weiss, '88;
Manley and Gleich, '91). Rose and Weiss ('88) suggest that
this population subserves auditory tasks that require tem-
poral precision, such as sound localization. These fibers
form an end bulb projection to the nucleus magnocellularis
similar to that described for birds. Fibers from the bidirec-
tional population, however, have higher characteristic fre-
quencies, show poorer synchronization to tones, and re-
spond to sound chiefly by an increase in discharge rate
(Weiss et al., '76; Manley et al., '90; Manley and Gleich, '91).
These fibers form bouton-like terminals in the medial
nucleus angularis. At present, there is little known about
the differences between the two parts of the nucleus
angularis. The division into functional timing and non-
timing pathways in lizards may be analogous to the division
into time and intensity pathways in birds. Lizards may have
independently developed the parallel processing of intensity
components of the auditory stimulus through development
of a new hair cell type.
Comparisons with mammalian auditory nerve
projections
Mammals have evolved high-frequency hearing, and it
seems probable that this development was responsible for
the substantial differences between the central auditory
system of mammals and that of the reptiles and birds. What
appears to have changed the least during phylogeny is the
system for encoding timing information. The mammalian
projection from low best-frequency auditory nerve fibers to
C.E. CARR AND R.E. BOUDREAU
bushy cells via an end bulb is homologous to the projection
described in birds and reptiles. In the alligator lizard, the
chicken, the barn owl, and the cat, each auditory nerve fiber
may form more than one end bulb, while each bushy cell or
magnocellular neuron receives 2-3 end bulbs (Boord and
Rasmussen, '63; Miller, '75; Rube1 and Parks, '75; Miller
and Kasahara, '79; Fekete et al., '82; Browner and Pierz,
'86; Rouiller et al., '86; Browner and Marbey, '88; Sento
and Ryugo, '89). There are also major differences between
mammals and the other amniote groups. Mammalian audi-
tory nerve fibers project to 3 cochlear nuclei, the anteroven-
tral, posteroventral, and dorsal cochlear nuclei. Further-
more, each auditory nerve fiber projects to many more
targets within the cochlear nuclei, indicating that there is
more parallel processing of the auditory signal in the cat
(Rhode et al., '83; Rouiller et al., '86).
Detailed information about the auditory nerve projec-
tions permits useful comparisons between the barn owl and
the cat, and testing of several hypotheses. In the cat, there
is a relationship between characteristic frequency and end
bulb size, where the largest end bulbs had characteristic
frequencies below 4 kHz. Since this discontinuity in end
bulb size occurs at the upper limit for phase-locking in the
cat, Rouiller et al. ('86) suggested that the large end bulbs
are specialized for phase-locking and sound localization.
The duplex theory proposes that mammals use the interau-
ral phase differences from low-frequency sounds to localize
sounds below 4 kHz, and the interaural intensity differ-
ences from higher-frequency sounds to localize sounds
above 4 kHz (Moushegian and Jeffress, '59; Hafter et al.,
'88). The barn owl does not use time and intensity informa-
tion in this duplex fashion, but in parallel, and no frequency-
related changes in end bulb size or percentage cover were
found in the barn owl. These observations from the barn
owl and the cat are therefore consistent with the hypothesis
that large end bulbs are selected for the encoding of
phase-locked spikes for detection of interaural phase differ-
ences.
A second hypothesis from the mammalian literature
concerns the convergence of several end bulbs onto a single
neuron. This has been observed in both the bushy cell
region of the mammalian anteroventral cochlear nucleus
(Lorente de No, '79; Brawer and Morest, '74; Cant and
Morest, '79; Ryugo and Fekete, '82; Sento and Ryugo, '89)
and in the barn owl. In the mouse, in vitro recordings from
bushy cells have shown that they receive several auditory
nerve inputs (Oertel, '83; Oertel et al., '88). In vivo intracel-
lular recordings from bushy cells in cat also indicate that
they may receive converging auditory nerve inputs (Rhode
et al., '83). It is not clear, however, that these converging
inputs function to improve phase-locking. It has been
suggested that they may mediate responses to more com-
plex auditory stimuli (Carney, '89). In the barn owl,
however, convergent auditory nerve inputs onto magnocel-
lular neurons may improve phase-locking (Sullivan and
Konishi, '84). Furthermore, in the barn owl, convergence is
not the result of an overabundance of auditory nerve fibers
sharing a small number of target magnocellular neurons,
but is created by each auditory nerve fiber dividing to form
3-6 end bulbs. Each fiber produces more end bulbs than is
the case in cats. The large number of end bulbs per
magnocellular neuron may be specializations for the high
temporal resolution of owl's auditory system.
OWL AUDITORY NERVE
SUMMARY
Specializations for the encoding of temporal information
include the robust end bulb synapses from the auditory
nerve to the nucleus magnocellularis. These features are
shared by all birds, reptiles, and mammals, and appear to be
conserved solutions for the preservation and coding of
temporally ordered signals in the auditory system. The
projections to the nucleus angularis are variable in all birds,
reptiles, and mammals. This variability may reflect the
different demands placed upon the intensity coding system
during phylogeny.
ACKNOWLEDGMENTS
We thank Dr. M. Konishi for making his expertise and
laboratory facilities available for the electrophysiological
experiments. The work was supported by NIH-DC 000436
and an Alfred P. Sloan fellowship.
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