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The Journal of Neurophysiology Vol. 79 No. 6 June 1998, pp. 3127-3142
Copyright ©1998 by the American Physiological Society
1 Department of Anatomy and 2 Department of Neurophysiology, University of Wisconsin Medical School, Madison, Wisconsin 53706; and 3 Division of Neurophysiology, Medical School, KULeuven, B3000 Leuven, Belgium
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Smith, Philip H., Philip X. Joris, and Tom C. T. Yin. Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J. Neurophysiol. 79: 3127-3142, 1998. We have recorded from principal cells of the medial nucleus of the trapezoid body (MNTB) in the cat's superior olivary complex using either glass micropipettes filled with Neurobiotin or horseradish peroxidase for intracellular recording and subsequent labeling or extracellular metal microelectrodes relying on prepotentials and electrode location. Labeled principal cells had cell bodies that usually gave rise to one or two primary dendrites, which branched profusely in the vicinity of the cell. At the electron microscopic (EM) level, there was a dense synaptic terminal distribution on the cell body and proximal dendrites. Up to half the measured cell surface could be covered with excitatory terminals, whereas inhibitory terminals consistently covered about one-fifth. The distal dendrites were very sparsely innervated. The thick myelinated axon originated from the cell body and innervated nuclei exclusively in the ipsilateral auditory brain stem. These include the lateral superior olive (LSO), ventral nucleus of the lateral lemniscus, medial superior olive, dorsomedial and ventromedial periolivary nuclei, and the MNTB itself. At the EM level the myelinated collaterals gave rise to terminals that contained nonround vesicles and, in the LSO, were seen terminating on cell bodies and primary dendrites. Responses of MNTB cells were similar to their primary excitatory input, the globular bushy cell (GBC), in a number of ways. The spontaneous spike rate of MNTB cells with low characteristic frequencies (CFs) was low, whereas it tended to be higher for higher CF units. In response to short tones, a low frequency MNTB cell showed enhanced phase-locking abilities, relative to auditory nerve fibers. For cells with CFs >1 kHz, the short tone response often resembled the primary-like with notch response seen in many globular bushy cells, with a well-timed onset component. Exceptions to and variations of this standard response were also noted. When compared with GBCs with comparable CFs, the latency of the MNTB cell response was delayed slightly, as would be expected given the synapse interposed between the two cell types. Our data thus confirm that, in the cat, the MNTB receives and converts synaptic inputs from globular bushy cells into a reasonably accurate reproduction of the bushy cell spike response. This MNTB cell output then becomes an important inhibitory input to a number of ipsilateral auditory brain stem nuclei.
Principal cells of the medial nucleus of the trapezoid body (MNTB) play a pivotal role in the processing of binaural information by brain stem auditory circuitry. As a result of their glycinergic nature (Bledsoe et al. 1990 Many of the methods used for these experiments have been described in detail elsewhere (Smith and Rhode 1985 Surgical procedure
Young adult cats were anesthetized and maintained in an areflexive state with pentobarbital sodium (35 mg/kg). Pinnae were removed, and the external auditory meati cut transversely for insertion of metal ear pieces through which acoustic stimuli, calibrated from 60 Hz to 40 kHz, were delivered. The MNTB was surgically approached from the ventral surface of the brain stem. A small hole was drilled in the basioccipital bone just lateral to the pyramidal tract, and a slit was made in the dura. The small rootlets of cranial nerve VI served as an external landmark for the more deeply located MNTB.
Acoustic stimuli and data collection
Calibrated acoustic stimuli generated by a computer-controlled digital stimulus system (Rhode 1976 Glass electrodes Intracellular glass electrodes were filled either with a buffered (pH 7.6), filtered 5% HRP (Sigma) solution in 0.5 M KCl or a 2% Neurobiotin (Vector Labs) solution in 0.5 M KCl. The electrode was lowered over the hole drilled in the skull and advanced in 1-µm steps. Extracellular and intracellular signals were monitored using standard techniques for DC monitoring, amplification, filtering, and display. Recordings from MNTB cells using the glass microelectrodes could only be verified by subsequent location and identification of the labeled cells. However, some features of axonal responses were used to distinguish presumed MNTB axonal responses from those of other axons: 1) because the primary excitatory input to a MNTB cell arises from a globular bushy axon from the contralateral cochlear nucleus, only units driven from the contralateral ear were considered. 2) Because of the interposing synapse between globular bushy axon and MNTB cell, first spike latencies taken from peristimulus time histograms (PSTHs) to STCFs should be slightly longer for a MNTB cell axon than for a bushy cell axon with the same characteristic frequency.
Metal electrodes Commercially available tungsten metal electrodes (Microprobe, 10-20 µM exposed tips, 5 M Tissue processing
For metal electrode experiments, we perfused the animal with formalin shortly after a lethal dose of pentobarbital sodium was administered after the last penetration. For the HRP/Neurobiotin experiments, the animal was maintained in an areflexive state for 24-36 h after the last penetration using a drip solution of sodium pentobarbital (3% in 5% dextrose) while heart rate, respiration, and withdrawal reflexes were checked every 20 min by one of the experimenters. Wound areas were swabbed at 2-h intervals with lidocaine. After a lethal dose of sodium pentobarbital, the cat then was perfused transcardially with saline followed by two concentrations of phosphate-buffered, calcium-containing glutaraldehyde:paraformaldehyde fixative (0.01:0.01 and 0.02:0.01), and the brain stored either in sucrose buffer (for frozen sectioning) or 1:1 glutaraldehyde:paraformaldehyde fixative (for vibratome sectioning).
Data analysis
PHYSIOLOGY.
When a cell or axon was isolated, stimuli were presented to each ear separately to determine which ear(s) drove the unit. For all cells, we determined the characteristic frequency (CF, the frequency at which the threshold intensity was the lowest), spontaneous discharge rate, and Q10 (CF/bandwidth at 10 dB above threshold) using an automated threshold tuning curve program. We also measured the STCF at 10- to 20-dB intervals from near threshold to 50-70 dB above threshold using 100 or 200 repetitions of 25-ms tones presented every 100 ms with a 3.9-ms rise/fall time. Amplitude-modulated and click stimuli also were used but the data will not be presented here.
ANATOMY.
Labeled axons were drawn in the coronal or horizontal plane using a camera lucida with ×63 oil objective. Measurements of the features of terminals on MNTB principal cell bodies and dendrites were quantified using a Summagraphics bit pad Two graphics tablet interfaced to the same microVax computer used to generate auditory stimuli.
General
The recording configurations used to collect the MNTB cell data described in this paper as well as to collect data from the globular bushy cells, which have been reported previously (Joris et al. 1994a
Anatomy
CELL BODIES.
Previous extracellular studies of the cat superior olivary complex (Guinan et al. 1972b DENDRITIC TREE.
Figure 3 illustrates the cell bodies and dendritic trees of our four well-labeled MNTB cells. Typically, the dendritic tree arose from one or two large main dendrites that branched rather profusely within a single compact area much like the dendritic trees of globular bushy cells in the cochlear nucleus, which provide the main excitatory input to these cells. In one instance, however, (Fig. 3, soma at middle left), a single MNTB cell body gave rise to two main dendrites, one with the compact morphology and the other branching occasionally over a fairly extensive area. This cell also displayed the highly unusual feature of two main axons arising from the cell body.
TERMINAL DISTRIBUTION.
At the electron microscopic (EM) level globular bushy cell calyceal terminals form the major input onto the MNTB principal cell body. Figure 4 illustrates one such calyx that has been labeled by intraaxonal injection of the globular bushy cell axon giving rise to the calyx, synapsing on an unlabeled MNTB principal cell (Fig. 4, A and B) and another unlabeled calyx synapsing on a MNTB cell labeled by intraaxonal injection of its axon (Fig. 4C). In selected EM sections, we measured the fraction of cell body and dendritic tree surface that was covered by synaptic profiles for three of the well-labeled, plastic-embedded cells (top 3 cells in Fig. 3). For the three cell bodies, 60.9, 66.6, and 68.4% of the total surface was covered with synaptic terminal profiles; 39.6, 43.8, and 48% of the surfaces were covered with terminals containing round vesicles, whereas 21.3, 22.8, and 20.4% of the surface were covered with terminals containing nonround vesicles. The remaining 39.1, 33.4, and 31.6% were terminal-free zones. The total amount of the surface of the proximal dendritic trees, within 100 µm of the cell body were also equally innervated with 65.9% of the total surface covered and 35.5% of the surface covered with terminals containing round vesicles. Synaptic coverage dropped precipitously on the distal dendritic tree (>100 µ from the cell body) where only 15% of the surface was terminal-covered and only 2% covered with round-vesicle containing profiles.
AXON.
Our well-injected axons indicate that the projection of an individual MNTB cell axon can be quite extensive innervating a number of auditory nuclei in the ipsilateral brain stem only. Figures 5-8 illustrate examples of projection patterns for labeled axons. The primary sites of innervation of our MNTB cell axons were the ipsilateral LSO and ventral nucleus of the lateral lemniscus (VNLL). In addition, collaterals often were seen with terminal swellings in periolivary regions, medial to the dorsal and ventral aspect of the MSO, which have been designated dorsomedial and ventromedial periolivary regions (DMPO and VMPO) (Spangler et al. 1985
Physiology
The primary excitatory inputs to MNTB cells are the large somatic calyceal terminals that arise from GBC axons. Thus it would seem appropriate to make comparisons of MNTB cell responses with those of GBCs that we have previously reported (Smith et al. 1991
Summary
We labeled eight MNTB cells intraaxonally after obtaining their physiological response properties. In agreement with previous qualitative anatomic descriptions (Jean-Baptiste and Morest 1975 Globular bushy cell input The data available from our MNTB cell sample show the results of what is apparently a good transmission of temporal information across the synapse. Globular bushy cells carry a variety of accurately timed information about low- as well as high-frequency auditory stimuli. Our previous reports (Joris et al. 1994a Globular bushy cell calyceal and other inputs
In our previous report (Smith et al. 1991 Calyceal and postsynaptic physiology
In addition to the anatomic specializations, some physiological specializations also apparently have developed both pre- and postsynaptically to aid in the secure and rapid transfer of accurately timed information. On the basis of whole cell patch recordings from calyceal terminals, the calyx possesses a large, high-voltage-activated calcium conductance with fast activation and deactivation kinetics (Borst et al. 1995 MNTB cell output
Our anatomic data on the projections of MNTB principal cells correspond well with Spangler et al. (1985)
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Sanes et al. 1987; Wenthold et al. 1987; Zarbin et al. 1981), these cells convert an excitatory signal, received from globular bushy cells (GBCs) in the contralateral cochlear nucleus, to an inhibitory signal. The inhibition is projected chiefly to the ipsilateral lateral superior olive (LSO), which also receives excitatory input from spherical bushy cells (SBCs) of the ipsilateral cochlear nucleus. Many LSO cells, then, are excited by stimulation of the ipsilateral ear and inhibited by stimulation of the contralateral ear. As a consequence, they become the initial point at which sensitivity to interaural level disparities is processed.
; Friauf and Ostwald 1988; Glendenning et al. 1985; Held 1893; Lenn and Reese 1966; Morest 1968; Smith et al. 1991; Spirou et al. 1990; Tolbert et al. 1982; Warr 1972). The size and somatic location of the calyx of Held recently has made it the focus of a considerable amount of interest in the cellular/biophysical neuroscience community where, for the first time in the CNS, whole cell patch-clamp recordings have been made from a presynaptic terminal, sometimes while simultaneously recording from the postsynaptic cell as well (Borst and Sakmann 1996; Borst et al. 1995; Forsythe 1994; Takahashi et al. 1996). The calyceal recordings showed the presence of specialized potassium and calcium conductances that would be appropriate for a synapse that has to accurately process high rates of spike activity (Borst et al. 1995; Forsythe 1994) but also indicated the existence of presynaptic metabotropic glutamate receptors that may act to modify the output of this terminal (Takahashi et al. 1996). Both in vitro sharp and patch electrode recordings from rodent MNTB cells (Banks and Smith 1992; Banks et al. 1993; Borst et al. 1995; Brew and Forsythe 1995; Forsythe and Barnes-Davis 1993a,b; Wu and Kelly 1991) indicates that the mature calyceal input acts primarily on non-N-methyl-D-aspartate glutamatergic receptors to generate a large, fast suprathreshold synaptic response. The rapid repolarization of the synaptic response, allowing these cells to follow their inputs at high rates, and the tendency of these cells to fire once to sustained depolarizing current are, in part, due to a dendrotoxin sensitive, low-threshold potassium conductance. A similar conductance has been reported for the bushy cells that provide the calyceal input to MNTB (Manis and Marx 1991; Oertel 1983; Wu and Oertel 1984). A second fast, high-threshold potassium conductance also is present in MNTB cells serving to rapidly repolarize the action potential (Brew and Forsythe 1995). Thus MNTB is part of an afferent chain with morphological and physiological specializations for temporally precise transmission of signals.
and subsequently labeledprincipal cells comes from the rat MNTB (Sommer et al. 1993). In this paper, the authors recorded intraaxonally from 11 MNTB principal cells and successfully injected them with horseradish peroxidase (HRP), labeling cell body and dendritic tree as well as much of the axonal field. However, the brief recording times allowed only a very limited measurement of the responses of these cells to auditory stimuli: the characteristic frequency (CF, the frequency at which the threshold intensity was the lowest) of only six cells was determined, and only 10 stimulus trials were used to generate short tone responses to the CF (STCF responses), making it impossible to determine their physiological response type, i.e., primarylike (PL; a response resembling auditory nerve fibers), primarylike-with-notch (PLN: a response resembling the globular bushy cell) or phase-locked (cells of low CF with spikes occurring at a particular phase of a low-frequency stimulus cycle). The remaining in vivo studies of MNTB have used extracellular metal electrodes (Guinan and Li 1990; Guinan et al. 1972a,b; Li and Guinan 1971; Tsuchitani 1994, 1997) and indirect evidence, the presence of a large prepotential, to identify the recorded cells. With metal electrode recordings, many cells in the vicinity of the MNTB exhibit spikes with complex waveforms, so-called prepotential cells. Based on similar recordings from the cochlear nucleus that were proposed to arise from the large auditory nerve endbulb of Held terminal/bushy cell complex (Pfeiffer 1966), Guinan and Li (1990) postulated that these waveforms arose from the calyx/MNTB principal cell complex and consisted of a prepotential in the presynaptic calyx followed by a postsynaptic spike. Responses to short tones from cells displaying such spike waveform were either primarylike, primarylike-with-notch or phase-locked. Subsequently Tsuchitani, (1994, 1997) categorized cells in the vicinity of MNTB as being MNTB principal cells based on the presence of a prepotential and/or a PL or PLN short tone response. Given the large number of fibers in the trapezoid body coursing directly through the MNTB with PL and PLN responses (Smith et al. 1991, 1993b), we believe the presence of a prepotential is essential for positive identification of extracellular recordings from MNTB cells. Furthermore, while it is generally thought that MNTB cells are monaurally driven by the contralateral ear, there are no documented interaural level difference functions in the literature for MNTB cells documenting this characteristic.
; Banks and Smith 1992; Kuwabura and Zook 1992; Kuwabura et al. 1991; Smith 1995; Sommers et al. 1993) that MNTB cells project to the medial superior olive (MSO), a nucleus containing cells that are thought to be comparing the time of arrival of the excitatory inputs from the two ears (Yin et al. 1997). All but one of these studies were in vitro so the auditory response features (CF, STCF response, spontaneous rate) of these MSO-projecting MNTB cells could not be assessed. In the one in vivo study (Sommers et al. 1993), no auditory responses were recorded from the one labeled MNTB cell that projected to MSO. The excitatory input to the MSO comes bilaterally from the spherical bushy cells of the anteroventral cochlear nucleus (AVCN), cells that exhibit enhanced synchronization as compared with their auditory nerve input to low CF tones (Joris et al. 1994a). It is essential to know the character of the inhibitory input to these cells from the MNTB if we are to understand the processing of interaural time disparities in the MSO and interaural level differences in the LSO.
; Lenn and Reese 1966; Morest 1968, 1973) described the calyceal ending and mentioned that there were other "noncalyceal terminals" on the cell body, but no measures were made of the extent of these terminals, and, because of the unlabeled nature of the cells, a description of the synaptic input to only the most proximal dendrites could be given. For the MNTB output, several light microscopic studies have described the projection pattern of MNTB axons in various species (Banks and Smith 1992; Kuwabura and Zook 1991, 1992; Schofield and Cant 1992; Sommer et al. 1992), but no electron microscopy was done to confirm or describe the terminal morphology. Cant (1984) reported that in the LSO (a major recipient of MNTB axon collaterals), almost three-fourths of the surface of the LSO principal cell body and proximal dendrites are covered with synaptic terminals that are almost exclusively those containing small vesicles many of which are flattened or cylindrical. She proposed that these terminals arose from MNTB axons but admitted that it remained to be demonstrated experimentally (Cant 1984). Thus the ultrastructural identification of the axon terminals of identified MNTB principal cells has never been unequivocally made.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
; Smith et al. 1991, 1993b) and are summarized here. Animals were maintained in an American Association for Accreditation of Laboratory Animal Care (AAALAC)-approved animal care facility, and all methods have been approved by the University of Wisconsin Institutional Animal Care And Use committee.
) were delivered from Telex 140 earphones or Radioshack supertweeters. Spike-triggered pulses were sent to a unit event timer and stored for on-line and subsequent analysis. As the electrode was advanced toward the MNTB, a search stimulus of short tone bursts with variable frequency was presented to both ears until an axon or a cell body was encountered.
recording and injection
30 to 60 mV, was accomplished with 100-ms current pulses. After physiological characterization of the cell (see further) HRP or neurobiotin was injected for 2-10 min using 100 ms, 1-5 nA current pulses while CF tones were presented continuously. Current injection was terminated if the response during pauses in the injection changed, which would indicate that the electrode had slipped into a different cell. After data collection, the electrode was withdrawn, the DC shift noted and a 10-mV calibration pulse recorded on the intracellular channel of the tape monitor.
recording
impedances) were used in separate extracellular experiments. Electrode placement, method of advance, stimulus presentation, and unit response characterization were as described above for glass electrodes. Metal electrode recordings from MNTB cells were distinguished by their prepotentials (Guinan and Li 1990; Guinan et al. 1972a,b; Li and Guinan 1971) and by subsequent histological location of the recording site from lesions made at several points in each penetration (except for 4 cells in 1 animal where histology was not available).
). For light microscopy, sections were mounted on glass slides, counterstained with cresyl violet, and coverslipped. For electron microscopy, vibratomed, HRP-reacted sections were fixed in 2% osmium tetroxide, dehydrated, and flat-embedded in plastic resin. After a camera lucida drawing of the injected axon was made, thin sections were taken, counterstained with uranyl acetate and lead citrate, and observed with a JOEL 100CX electron microscope.
DAB-nickel/cobalt intensification method then prepared for light and/or electron microscopy as described above.
), mean coefficient of variation over the interval 12-18 ms (Young et al. 1988), and the sustained discharge rate and synchronization coefficient (Goldberg and Brown 1969) during the last 15 ms of the tone burst. To correct for spontaneous activity in the computation of the mean and standard deviation of the first spike latency, we eliminated all spikes in the time window from 0 to 2.4 ms after stimulus onset and all trials in which a spike occurred in the last half of this window.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
; Smith et al. 1991) and which are used here for comparative purposes, are illustrated in Fig. 1, top.
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FIG. 1.
Top: diagrammatic representation of the recording configurations from a medial nucleus of the trapezoid body (MNTB) principal cell or its globular bushy cell input. Globular bushy cell axons were recorded extra or intra-axonally, on the same or opposite side as the MNTB that they innervated, as previously described (Joris et al. 1994a ; Smith et al. 1993b). MNTB cells were recorded from either intra-axonally with glass electrodes or extracellularly, with metal electrodes in the vicinity of the presynaptic calyx/postsynaptic cell body complex. Bottom: extracellular metal electrode recordings from the MNTB. Waveform showed a prepotential (P.P.) presumed to arise from the calyx, followed by a MNTB cell action potential. Lower 2 traces: sound-driven MNTB action potentials, preceded by a prepotential, are superimposed on a trace, taken in the absence of intentional sound stimuli, showing no prepotential (No P. P.). Scales at top of columns apply to all traces in that column.
) and that were subsequently localized to the MNTB by electrode-generated lesions at the recording site. Typical complex waveforms recorded by extracellular metal electrodes in the MNTB are shown in Fig. 1. They usually consisted of a negative-going prepotential, that varied in amplitude from unit to unit, followed ~0.5 ms later by a larger bipolar spike, which was used to trigger the unit event timer. Although sound-driven spikes always were preceded by a prepotential, spontaneously occurring spikes (those not generated by our sound system) unaccompanied by a prepotential were occasionally seen (n = 3 cells; see Fig. 1, bottom 2 panels).
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FIG. 2.
Normalized short tone interaural level difference (ILD) functions for 4 cells localized to the MNTB that displayed prepotentials (encompassed by shaded area below "MNTB") and 9 cells localized to the lateral superior olive (LSO; encompassed by shaded area next to "LSO"). Tones at CF were used for all cases shown. For the MNTB recordings, contralateral stimulus was held constant 20-30 dB above threshold while the intensity of the ipsilateral stimulus was varied around 0 ILD. For the LSO cells, we held the ipsilateral level constant at 20-30 dB above threshold and varied the contralateral level.
) indicated that the MNTB is tonotopically organized, with low CF cells placed laterally and higher frequencies situated progressively more medial with isofrequency strips angled dorsomedially to ventrolaterally. We found the absolute location of our labeled MNTB cell bodies within the boundaries of the nucleus hard to quantify. The MNTB boundaries are often difficult to distinguish especially when sections are embedded in plastic but, in general, our data would seem to concur with this map. One labeled cell with a very high CF was situated very medially, embedded in VIth nerve axon bundles. A single, labeled low best-frequency cell was located considerably laterally and our other labeled cells with intermediate CFs were located between these two extremes.
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FIG. 3.
Camera lucida drawings of 4 labeled MNTB cells. Three cells on the left are drawn in the horizontal plane, whereas the cell on the right is drawn in the coronal plane. *, swelling where the electrode penetrated the axon and the axon distal to the recording site is much thinner than the axon between the injection site and the cell body. Scale bar at top right applies to all cells.
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FIG. 4.
A: electron micrograph of an unlabeled MNTB principal cell receiving synaptic input from an intraaxonally labeled globular bushy cell axon. In thin section, the fingerlike tendrils of the calyceal terminal are cut in cross-section (*). B: micrograph of the same MNTB cell at a level where the labeled globular bushy axon (curved dark arrows) loses its myelin sheath (curved open arrow) close to the origin of the calyx, then surrounds the cell in a "hand-gripping-a-ball"-like fashion, making multiple synaptic contacts (*). C: micrograph of MNTB cell labeled by intraaxonal injection. A large unlabeled terminal (curved arrows) containing round vesicles is presumably part of the globular bushy calyceal terminal. Scale bar in C = 5 µm and refers to all micrographs.
, 1987). In some cases, these axons also had collaterals to MSO and the MNTB itself.
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FIG. 5.
Camera lucida recontruction of a high (17.7 kHz) characteristic frequency principal cell, in the right MNTB, sectioned in the coronal plane (see also Fig. 3). Top left: higher power drawing of the cell body, dendritic tree and initial portion of the axon. *, penetration site of the electrode. Bottom left: low power reconstruction of the same cell and its axon collateral field. Location of some of the innervated nuclei appear out of place on this 2-dimensional drawing because of the large rostro-caudal distance traversed by the axon. Axon gave off numerous collaterals innervating an appropriate frequency region of the LSO [given the characteristic frequencies (CF)], MNTB, dorsomedial and ventromedial periolivary regions (DMPO and VMPO), and ventromedial region of the ventral nucleus of the lateral lemniscus (VNLL) before fading in the LL. Bottom right: short tone response of this cell at its CF (see also Fig. 10).
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FIG. 8.
Camera lucida of another MNTB cell in the horizontal plane. CF of the cell was 6,300 Hz. Left: drawing of cell body (CB) dendritic tree and the axon collateral system. Cell body and dendritic tree of this cell also are illustrated in Fig. 3. Scale bar = 500 µm. Middle: low power reconstructions of 3 horizontal sections of the right superior olivary complex representing the dorsal, intermediate, and ventral aspects of the LSO (top to bottom). Asterisk and arrows in top drawing indicate the dorsal course of the MNTB cell collateral as it enters the LSO. Middle and bottom: shaded portions of the LSO indicate the location of MNTB collateral branching and terminal swellings within the LSO. Scale bar = 2 mm. Right: higher power reconstruction of the MNTB axon collateral and branches within the LSO. Scale bar = 100 µm.
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FIG. 6.
Right: camera lucida reconstruction of a low (635 Hz) characteristic frequency MNTB cell, located in the right MNTB, sectioned in the coronal plane. Cell body was lightly stained and only the main dendrite and 2nd-order branches could be seen so the dendritic tree is not illustrated. Axon sent collaterals into the low-frequency, lateral limb of the LSO as well as into the dorsal, low-frequency region of the medial superior olive (MSO) at the 2 rostrocaudal locations illustrated. Branches were also seen in the VMPO. A number of collateral branches appeared to fade before termination, so this cell may have innervated other areas as well. Two profiles of the MSO represented are from 2 sections that contained collateral branches in this nucleus at 2 rostrocaudal locations. LSO profile represents the outline of the LSO in the section that contained the bulk of the collateral branches in the lateral limb of the LSO. Thus only these parts of the axon collateral branches are placed accurately in the drawing relative to the illustrated locations of the LSO and MSO. Scale bar = 500 µm. Inset, bottom left: short tone response of this cell at its characteristic frequency (see also Fig. 10).
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FIG. 7.
Camera lucida drawings of 2 MNTB cells in the horizontal plane illustrating the extent of the axon collateral fields. Cell body of the cell on the left (CB) was located in the left MNTB. CF of the cell was 27 kHz. Dendritic tree of this cell has not been drawn in this figure, to eliminate confusion of dendrites with axon collateral branches, but is illustrated in Fig. 3 (top left cell). Destination of the main axon branches are indicated (to LSO, to VNLL). Other collaterals are in MNTB and VMPO. Cell body of the cell on the right (CB) was located in the right MNTB. CF of the cell was 13 kHz. Destination of main collaterals are indicated (to LSO, to VNLL). Collateral branches between the cell body and the to-LSO label are primarily in the MSO. Enlarged version of the cell body and dendritic tree of this cell are illustrated in Fig. 3 (bottom left). Scale bar = 1 mm.
), these represent measurements of the axoplasm and do not include the myelin sheath and may be complicated by a number of factors. In the vicinity of the cell body, the axon diameter appeared to be quite large. Before beginning to give off its major collaterals, the axon diameter was usually between 4 and 6 µm. After beginning to branch, the major collaterals that, for example, headed laterally to LSO or rostrally toward VNLL were typically 3-4.5 µm and maintained this diameter until approaching near to the nucleus. Subsequent secondary branching of one of these main collaterals, for example when the major collateral projecting to the LSO began giving off major branches soon after entering the hilus, were usually 1.5-3 µm.
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FIG. 9.
A: electron micrograph of an unlabeled cell in the LSO (lso cell) receiving a labeled MNTB synaptic terminal on the cell body (curved arrow) and a primary dendrite (d, curved arrow). B: micrograph of the myelinated MNTB axon collateral (a) that gave rise to the labeled terminal (*) on the LSO cell dendrite (d). C: labeled MNTB axon terminal (*) on the cell body of the LSO cell (cb). Scale bar in A = 5 µm. Scale bar in B = 1 µm and applies to B and C.
).
1 to 53 dB for GBCs. Short tone responses were, in general, similar to GBC responses with some noticeable variations. Figure 10 shows PSTHs from representative MNTB cells over the entire frequency range and may be compared with the globular bushy cell response (Fig. 1 of Smith et al. 1991). More than 1 kHz the onset component of the MNTB response often would be well timed at higher stimulus intensity levels giving the response a PLN appearance. In some instances, however, the onset portion did not become well timed at any level (Fig. 10, bottom left and 4th trace in right column). We also occasionally noted what appeared to be a slight "sag" in the sustained portion of the short tone response (Fig. 10, bottom left and middle trace in right column).
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FIG. 10.
Representative short tone responses from axons of positively identified MNTB cells (*) or cells showing prepotentials in extracellular recordings localized to the MNTB, for a wide range of characteristic frequencies. Responses are to 200 tones (25 ms each) at the characteristic frequency of the unit, which is indicated at the top right of each panel. *, cell was labeled. Decibel value below the CF is the level above threshold that the tones were presented. Bin width = 0.1 ms.
) and intraaxonally (
) recorded MNTB cell population compared with the same data from our labeled globular bushy cell population. A number of comparisons may be made between populations. First, only a few of the MNTB cells had CFs <3 kHz (2/45) while this CF was represented much more extensively in our GBC population [~4% for MNTB cells vs. 12/35 (34%) for GBCs]. Those two MNTB cells with CFs <3 kHz had spontaneous rates of 0 spikes/s as did most of the GBCs population with such CFs (8/12 with 0 spikes/s and 11/12 <5 spikes/s). More than 3 kHz, the spontaneous rates tended to be higher for both MNTB cells and GBC populations (mean = 27 spikes/s vs. 12.4 spikes/s, respectively). If the boundaries chosen in the auditory nerve by Liberman (1978) are used for distinguishing high, medium, and low spontaneous rates (SRs) (18 and 1 spikes/s, respectively), the percentages of high, medium, and low SRs in MNTB cells were 55, 27.5, and 17.5%, respectively, compared with 23, 46, and 31% for GBCs and 65, 20, and 15% for auditory nerve (AN).
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FIG. 11.
Comparison of the spontaneous activity (top), 1st spike latency (middle), and 1st spike standard deviation (bottom) between labeled globular bushy cells, that we have previously reported (Smith et al. 1991 ) and MNTB cells. Labeled MNTB cells (MNTB) were recorded from intraaxonally. Unlabeled MNTB cells recordings using metal electrodes (PP) were identified based on the presence of a prepotential (see Fig. 1) and subsequent location of an electrode generated lesion site within the confines of the MNTB. Globular bushy cells axons were either recorded on the side ipsilateral or contralateral to their parent cell body.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Lenn and Reese 1966; Morest 1968, 1973), our measurements show that calyceal coverage can take up one-fourth to one-half of the total surface of the cell body and primary dendrites. In addition, we have shown that nonexcitatory inputs also concentrate on the cell body and consistently cover around one-fifth of the surface, but the source of this input or means of activation is unknown. Our data also show that inputs with both excitatory and inhibitory features are rare on the distal dendritic tree. We also have shown for the first time at the ultrastructural level that the terminals of these MNTB axons contain nonround vesicles and, when observed in the LSO, terminate on the somata and primary dendrites of LSO principal cells.
; Kuwabura and Zook 1991, 1992; Schofield and Cant 1992; Sommer et al. 1992; Spangler et al. 1985), MNTB cells send their axonal projections only to areas of the ipsilateral brain stem, namely (in cat) the ventral nucleus of the lateral lemniscus, the lateral and medial superior olives, the dorsomedial and ventromedial periolivary nuclei, and the MNTB. The only previous in vivo intracellular study (Sommer et al. 1992) indicated that the rat LSO receives MNTB inputs with best frequencies from 47 kHz down to 
14 kHz. Our labeled cells show that, in the cat, this frequency range extends down to 635 Hz. In addition, despite an admittedly small sample, our labeled cell data provides evidence that the MNTB projection to the MSO may be frequency specific-cells with CFs below <13 kHz innervate the MSO, cells with CFs >13 kHz do not.
. By stimulating either LSO or DMPO while recording a complex spike unit in the MNTB, they could antidromically activate a spike, designated the "A" spike. This A spike resembled the portion of the complex waveform, designated the "C2" component, that was believed to be the postsynaptic MNTB cell spike. When the complex spike was activated by stimulation of the trapezoid body at the midline, thus driving the globular bushy axon/calyceal synapse and presumably activating the MNTB principal cells, the antidromic A spike was refractory and could not be driven for ~1 ms, implying that the A spike and C2 component were both generated by the MNTB cell. We felt that this evidence, together with our positive identification of MNTB principal cells with physiology comparable to the complex waveform units, was sufficient to permit our inclusion of the extracellular data.
a comparison of responses
; Smith et al. 1991) have shown that low-frequency globular bushy cells can phase lock to the stimulus waveform of a short tone at their CF with remarkable precision (as measured by the synchronization coefficient) and often will entrain (generate a spike for every cycle of the stimulus waveform). Because our sample of MNTB cells with CFs <1 kHz is so small, it is difficult to compare GBC and MNTB cell populations in terms of phase locking capabilities. Nevertheless the positively identified MNTB cell with a CF <1 kHz showed "enhanced" synchrony, i.e., its maximum synchrony (0.89) was high relative to that of most auditory nerve fibers at that frequency. Also, maximum synchronization for the one MNTB cell in our sample with a CF between 1 and 3 kHz was at the lower edge of the range observed in the auditory nerve. These observations are consistent with synchronization in GBCs, which also show enhanced synchronization at CFs <1 kHz and poor synchronization at intermediate CFs (1 kHz < CF < 3 kHz). GBCs with CF >3 kHz show enhanced synchronization to tones in the low-frequency tail of the tuning curve (Joris et al. 1994b), but we did not test this in MNTB cells. As seen in Fig. 10, the onset component of the MNTB cell responses was well timed, although as a population not as well timed as globular bushy cells (Fig. 11C). Finally, GBC and MNTB cells show a slight improvement in envelope phase-locking compared with the auditory nerve, and overall the two populations are indistinguishable in their envelope phase-locking properties (Joris and Yin, unpublished data).
indicates that low frequencies are less well represented than higher frequencies in MNTB, 4% is probably not a true reflection of the actual number of MNTB cells with CFs <3 kHz but is probably biased by our surgical approach and electrode placement. In these experiments, the electrode was inserted into the brain stem just lateral to the pyramidal tract. In some instances, the electrode entered the brain near the rootlets of the abducens nerve perpendicular to the surface of the brain. Using this approach the more laterally situated, lower frequency regions of the MNTB are not traversed. Even when we angled the electrode so that it diverged from the midline with increasing depth the lateral aspect of the MNTB was often still not reliably sampled. This would probably also explain the disparity in mean spontaneous rates between our GBC (12.4 spikes/s) and MNTB cell (27 spikes/s) populations. Many of the low CF globular bushy cells we labeled with CFs <3 kHz had spontaneous rates of 0 spikes/s. Our two examples of MNTB cells with CFs <3 kHz also had spontaneous rates of 0 spikes/s, and it is likely that, had we sampled a higher percentage of low CF MNTB cells, the means would be closer.
), we noted that the labeled calyx of a globular bushy cell axon covered ~24% of its postsynaptic MNTB cell body surface, while the total (labeled and unlabeled) round vesicle coverage of the cell body was 26.4%. In this case, the great majority of the excitatory input was the labeled calyx, providing evidence that this cell received only one calyx. In the present study, the total round vesicle terminal coverage for three of our labeled MNTB cell bodies was 39.6, 43.8, and 48%. What does this say about the excitatory synaptic input to the MNTB cell body? 1) In the four cases, we have examined in detail the extent of somatic coverage by excitatory terminals has varied considerably, ranging from slightly more than one-fourth to slightly less than one-half. Thus if each MNTB cell is receiving only one calyx, then there may be considerable variation in amount of surface of MNTB cells covered by one globular bushy calyceal terminal. 2) Alternatively, some MNTB cells receive two calyces or 3) some MNTB cells receive one calyx and a lot of other noncalyceal round vesicle inputs. These could potentially arise from the small "precalycean" terminals of other globular bushy cell axons that make smaller terminal endings in the MNTB (Morest 1968; Smith et al. 1991). The axons of other projection neurons of the cochlear nucleus, with round vesicle containing terminals, do not venture into the MNTB so they are unlikely sources for additional excitatory inputs. These include the spherical bushy cells (Smith et al. 1993b), the stellate cells the axons of which exit the cochlear nucleus via the trapezoid body and that respond in a chopper fashion to short tones (Smith et al. 1993a), the octopus cells of the posteroventral cochlear nucleus (PVCN) and the giant and fusiform cells of the dorsal cochlear nucleus (DCN) (Joris et al. 1992). Little information is available on the other potential sources of excitatory inputs to MNTB in the brain stem. Labeled MSO principal cells in the guinea pig (Smith 1995) never gave off collaterals to MNTB, and there is only one report of an occasional projection to MNTB from labeled rat LSO principal cell the axon of which crossed the midline (Banks and Smith 1992).
) was 21.6%, and 21.3, 22.8, and 20.4% for the three cells in the present study. Thus it would appear that the presumably inhibitory "nonround vesicle" input to the soma is quite heavy and, at least in terms of surface coverage, is constant from cell to cell. Anatomically, it has been shown in cat and guinea pig that glycine immunoreactive terminals are rather sparse in the MNTB (Adams and Magnaini 1990; Helfert et al. 1989; Wenthold et al. 1987) as is glycine receptor labeling (Zarbin et al. 1981) while 
-aminobutyric acid (GABA) immunoreactive terminals are quite numerous (Adams and Magnaini 1990). This agrees with our observations here and similar observations in the rat (Banks and Smith 1992) that the MNTB cells, which are the major source of glycinergic innervation to the auditory brain stem, only give off occasional sparsely branching collaterals within the home nucleus. Little evidence is available as to the source of any of the GABAergic terminals nor is there evidence as to whether they are activated by auditory stimuli. Kuwabura et al. (1991) described axon collaterals of cells in the rodent ventral nucleus of the trapezoid body that could branch in MNTB, but it is not known what transmitter these cells manufacture. In vitro physiology in the mouse has shown that bath application of either GABA or glycine decreases the input resistance in only about half of the mouse MNTB cells tested (Wu and Kelly 1995). Further in vitro data indicated that shock stimulation of the trapezoid body at the midline or ipsilateral to the MNTB in the rat (Banks and Smith 1992) but not the mouse (Wu and Kelly 1991) would occasionally evoke inhibitory postsynaptic potentials (IPSPs) that could be blocked by the glycine antagonist, strychnine. Our in vivo data on the response of MNTB cells to binaural stimulation as the sound to the contralateral ear was held constant while the sound to the ipsilateral ear was increased (Fig. 2) showed no inhibitory affects on the contralaterally driven output. In other in vivo experiments, Guinan and Li (1990) also could not demonstrate any sort of inhibitory affect on the calyceal driven MNTB cell output either by auditory stimulation to either ear or by shock stimulation of the trapezoid body. Some of our MNTB short tone responses show an apparent sag in the sustained response (Fig. 10), but it would be premature to propose an inhibitory input as the cause. Thus inhibitory inputs on MNTB cells appear to be present and functional but there is no evidence of activation by simple auditory stimuli.
) that would be required for rapid synaptic transmission. In addition, preliminary reports (Forsythe 1994) showed that, in current clamp, the presynaptic terminal can spike at high rates in response to depolarizing current pulses because of a fast delayed rectifier potassium current that allows rapid spike repolarization. Such a rapid response capability also might be requisite for rapid synaptic transmission. The synaptic current generated postsynaptically by the calyx is fast and very large, averaging ~5 nA (Borst and Sakmann 1996), but this current amplitude diminished significantly during repetitive stimulation such that the calyceal synapse could not make the MNTB cell fire reliably to a 100-Hz shock stimulation of the bushy cell input. It would appear, however, that such poor postsynaptic following is probably a function of the immature preparation used (8- to 10-day-old rats) because shock rates of the bushy cell input generating MNTB cell spikes were reliably followed to well over 500 Hz in a mature mouse slice preparation (Wu and Kelly 1993). Postsynaptically the MNTB cell has specialized potassium conductances (Banks and Smith 1992). One has been designated ITEA, which might allow for rapid spike repolarization, the other IDTX, which might permit only a single spike to occur in response to the huge calyceal input (Brew and Forsythe 1995).
. With one exception, all axons that could be followed to LSO innervated that structure in a fashion that was consistent with the proposed frequency map of the LSO (Guinan et al. 1972b). Our one example of a low-frequency MNTB cell sending a projection to the low frequency limb supports the contention (Finlayson and Caspary 1991; Joris and Yin 1995) that some low-frequency LSO cells are inhibited by contralateral stimulation.
reported that almost three-fourths of the surface of the LSO principal cell body and proximal dendrites are covered with synaptic terminals that are almost exclusively those containing small vesicles many of which are flattened or cylindrical. Our labeled synaptic terminals from identified MNTB principal cells correspond to the description both in location and vesicle content (Cant 1984) and provide the first direct evidence that these terminals are derived from axons of MNTB cells. In the rat, Moore and Caspary (1983) showed that the contralaterally evoked inhibition of ipsilaterally evoked excitation could be blocked by application of the glycine antagonist strychnine. Similar results were obtained in the slice preparation, by Wu and Kelly (1991), with IPSPs evoked by electrical activation of MNTB. Thus our anatomic data, showing that the axon terminals of MNTB cells to the LSO have nonround synaptic vesicles, provide an important piece of data linking the presumed inhibitory function of MNTB onto ipsilateral LSO to the anatomic data of Cant (1984) showing flattened vesicles on the soma and proximal dendrites of LSO cells.
and Schwartz (1980) have reported the presence of terminals with flattened vesicles on principal cells in cat MSO. The innervation of MSO by MNTB cells also has been noted anatomically in rat, bat, mouse, gerbil, and guinea pig (Banks and Smith 1992; Kuwabura and Zook 1991, 1992; Smith 1995), and IPSPs, evoked by MNTB shock, in MSO principal cells were blocked by strychnine (Grothe and Sanes 1993, 1994; Smith 1995), confirming the glycinergic nature of the input. The function of such an actively driven inhibitory input to the MSO from MNTB remains speculative. Several possibilities include a MNTB input the CF of which is slightly off the CF of the innervated MSO cell could serve to suppress coincident excitatory inputs at non-CF frequencies; mediation of precedence-like effects; and changing the MSO cells resting membrane potential during contralateral ear stimulation.
), so, as with the VNLL, we again note a region receiving both a contralateral excitatory input from cochlear nucleus and an inhibitory input from MNTB, a nucleus that is driven by contralateral excitatory input. The rodent superior paraolivary nucleus (SPN) is a large periolivary nucleus dorsomedial to the MSO that is considered the homolog of the cat DMPO. It receives input from both cochlear nuclei (Thompson and Thompson 1991) as well as a strong topographic input from MNTB principal cells (Banks and Smith 1992), and its cells project primarily either to the inferior colliculus or cochlear nucleus (Schofield 1991). Although some extracellular recordings were done in vivo on cells in the gerbil SPN and cat DMPO (Guinan et al. 1972a; Spitzer and Semple 1995), the physiology of a large population of cells in this nucleus has never been explored in great detail and consequently the possible effects of the MNTB input, on auditory response properties of cells here, are not known. We also occasionally noted a collateral being given off within the MNTB and, as noted above, inhibitory synaptic events can be elicited in rat MNTB cells by shocking their bushy cell input (Banks and Smith 1992), but it is not clear that these were due to collaterals of MNTB cells.
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ACKNOWLEDGEMENTS |
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This work was supported by National Institutes of Health Grants DC-01999 and DC-00116 and National Science Foundation Grant BNS-8901993.
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FOOTNOTES |
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Address for reprint requests: Philip Smith, Dept. of Anatomy, University of Wisconsin Medical School, Madison, WI 53706.
Received 3 November 1997; accepted in final form 20 February 1998.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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