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Powerful, Onset Inhibition in the Ventral Nucleus of
the Lateral Lemniscus
David A. X. Nayagam, Janine C. Clarey and Antonio G. Paolini
J Neurophysiol 94:1651-1654, 2005. First published 7 April 2005; doi:10.1152/jn.00167.2005
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J Neurophysiol 94: 1651–1654, 2005.
First published April 7, 2005; doi:10.1152/jn.00167.2005.
Report
Powerful, Onset Inhibition in the Ventral Nucleus of the Lateral Lemniscus
David A. X. Nayagam,1,2 Janine C. Clarey,1 and Antonio G. Paolini3
1
The Bionic Ear Institute, East Melbourne, Victoria; 2Department of Otolaryngology, The University of Melbourne,
East Melbourne, Victoria; and 3School of Psychological Science, LaTrobe University, Bundoora, Victoria, Australia
Submitted 16 February 2005; accepted in final form 1 April 2005
termed onset-ideal (OI). This response pattern is a result of the
detection of synchrony in auditory nerve fiber inputs representing a wide range of characteristic frequencies (CFs) (Golding
et al. 1995; Oertel et al. 2000). The function of these cells and
their projection to the VNLL is unknown, although they seem
well suited to encode onsets, transients, and temporal features
of complex, periodic stimuli (Oertel and Wickesberg 2002).
The role of the VNLL’s projection to the IC (Kelly et al. 1998;
Merchán and Berbel 1996), which is inhibitory (Batra and
Fitzpatrick 2002; Oertel and Wickesberg 2002) is equally
uncertain. We used in vivo intracellular recordings to investigate how VNLL cells utilize this well-timed onset information.
METHODS
Various lines of evidence indicate that inhibition plays as
important a role as excitation in controlling spike timing in
auditory nuclei (Brand et al. 2002; Casseday et al. 2000, 1994;
Wehr and Zador 2003). One of the major inhibitory pathways
within the auditory brain stem originates in the ventral nucleus
of the lateral lemniscus (VNLL) (Saintmarie and Baker 1990;
Zhao and Wu 2001), a nucleus thought to play a role in
temporal pattern processing (Covey and Casseday 1999; Oertel
and Wickesberg 2002). This structure is a crucial integration
site for a subset of fibers from the lower auditory brain stem en
route to the inferior colliculus (IC) (Covey and Casseday 1999;
Oertel and Wickesberg 2002; Wu 1999). VNLL neurons receive convergent excitatory input from a variety of cell types
within the contralateral cochlear nucleus (CN) (Glendenning et
al. 1981; Zhao and Wu 2001), including an exclusive projection from the octopus cell area (OCA) of the contralateral CN
(Adams 1997; Schofield and Cant 1997). Octopus cells give
rise to thick axons that terminate in large calyx-like synapses,
akin to endbulbs of Held in other auditory nuclei (Adams 1997;
Schofield and Cant 1997). These characteristics suggest that
this pathway provides fast and faithful transmission of timing
information (Batra and Fitzpatrick 1999; Zhao and Wu 2001).
Octopus cells respond to the onsets of sounds with exquisitely
timed responses (Godfrey et al. 1975; Rhode and Smith 1986),
Experiments were performed on 26 male Hooded Wistar (pigmented) rats weighing between 250 and 360 g. Animals were anesthetized with intraperitoneal aqueous urethan (20% wt/vol: total dose:
2.6 g/kg; Sigma, Sydney, Australia), and supplementary doses were
administered during the experiment if a corneal or paw reflex was
observed. Some animals were initially sedated with isoflurane (4 –5%
in 2% O2) prior to injection of urethan. The animal’s temperature was
maintained at ⬃37.5°C by a thermostatically controlled heating pad.
At the end of the recording session, the animal was intra-cardially
perfused with 10% formalin. Brains were removed, postfixed in 10%
formalin, and sectioned on a freezing sledge microtome (100 ␮m
sections). Sections were stained for Nissl substance using thionin, and
standard histological procedures were used to reconstruct and verify
the location of electrode tracks and recorded units (Paolini et al.
2001). Reconstructed recording depths were referenced to the cortical
surface as well as the point at which the electrode broke when it hit the
pia underlying the ventral brain stem (Paolini et al. 2001). A dramatic
drop in microelectrode impedance indicated this breaking point. All
procedures were in accordance with the Royal Victorian Eye and Ear
Hospital Animal Research Ethics Committee guidelines (project approval codes 95/037 and 04/104A).
Once the animal was deeply anesthetized, it was placed in a
stereotaxic frame, and a pinhole craniotomy (area: ⬃4 mm2) was
made using stereotaxic coordinates (Paxinos and Watson 1998) and
skull suture landmarks as guides. Recording micropipettes were inserted dorsoventrally into the left hemisphere and traversed the cerebral cortex and IC before encountering the lateral lemniscus and its
dorsal and ventral nuclei.
Intracellular neural responses were recorded using quartz glass
micropipettes (1.0 mm OD, 0.7 mm ID, Sutter Instruments, Novato,
CA), filled with 1 M potassium acetate and with impedances ranging
from 30 to 70 M⍀. The amplified (Axoclamp 2B amplifier, Axon
Instruments, Union City, CA) and filtered signal (output bandwidth ⫽
1 kHz) from the microelectrode was played through a speaker and
displayed on a Tektronix 465 storage oscilloscope (Beaverton, OR).
Address for reprint requests and other correspondence: A.G. Paolini, School
of Psychological Science, La Trobe University, Bundoora, Victoria 3086,
Australia (E-mail: [email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked “advertisement”
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
INTRODUCTION
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Nayagam, David A. X., Janine C. Clarey, Antonio G. Paolini.
Powerful, Onset Inhibition in the Ventral Nucleus of the Lateral
Lemniscus. J Neurophysiol 94: 1651–1654, 2005. First published
April 7, 2005; doi:10.1152/jn.00167.2005. The function of the ventral
nucleus of the lateral lemniscus (VNLL), a secondary processing site
within the auditory brain stem, is unclear. It is known to be a major
source of inhibition to the inferior colliculus (IC). It is also thought to
play a role in coding the temporal aspects of sound, such as onsets and
the periodic components of complex stimuli. In vivo intracellular
recordings from VNLL neurons (n ⫽ 56) in urethane anesthetized rats
revealed the presence of large-amplitude, short-duration, onset inhibition in a subset of neurons (14.3%). This inhibition occurred before
the first action potential (AP) elicited by noise or tone bursts, was
broadly tuned to tonal frequency and was shown to delay the first AP.
Our data suggest it is a result of an intrinsic circuit activated by the
octopus cell pathway originating in the contralateral cochlear nucleus;
this pathway is known to convey exquisitely timed and broadly tuned
onset information. This powerful inhibition within the VNLL appears
to control the timing of this structure’s inhibitory output to higher
centers, which has important auditory processing outcomes. The
circuit also provides a pathway for fast, broadly tuned, onset inhibition to the IC.
Report
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D.A.X. NAYAGAM, J. C. CLAREY, AND A. G. PAOLINI
RESULTS AND DISCUSSION
Intracellular recordings from 56 VNLL neurons revealed
that a subset (14.3%; 8/56) showed contralaterally evoked
inhibitory post synaptic potentials (IPSPs) before the first AP
elicited by noise and tones (Fig. 1A). These monaurally driven
IPSPs were large amplitude with a mean of 8.0 ⫾ 1.8 (SE) mV
and ranged between 3.7 and 19.1 mV. There was no relationship between IPSP amplitude and resting membrane potential
(RMP) in these cells (r ⫽ 0.05; P ⬎ 0.05; mean RMP ⫽
⫺48 ⫾ 4 mV.) In response to noise bursts, the average latency
of maximum hyperpolarization was 5.6 ⫾ 0.3 ms (Fig. 1D,
white bars), and the AP in these cells occurred with a mean first
spike latency (FSL) of 8.5 ⫾ 1.0 ms (Fig. 1D, black bars). The
inhibition showed a fast and reliable time course. In two cells
that displayed spontaneous IPSPs, of similar magnitude to the
stimulus evoked IPSP, it was possible to observe the full
inhibitory time course of ⬃8 ms (Fig. 1C). The inhibition was
also broadly tuned to tonal frequency (Fig. 1B).
J Neurophysiol • VOL
FIG. 1. Onset inhibition in ventral nucleus of the lateral lemniscus (VNLL)
neurons. A: in vivo intracellular responses recorded from a VNLL neuron to
contralaterally presented noise bursts (80 dB RMS; 20 trace overlay, lighter
gray) and a characteristic frequency (CF) tone burst (80 dB SPL; single trace,
darker gray). Horizontal dashed line indicates the mean resting membrane
potential (RMP; ⫺47 ⫾ 4 mV). The arrow indicates membrane hyperpolarization and the horizontal bar indicates stimulus duration. B: single traces to
off-CF tone bursts. Horizontal bar indicates time scale from stimulus onset. C:
spontaneous inhibitory postsynaptic potentials (IPSPs) were also observed in
this cell (black trace) and are compared with the onset component of a single
noise response (gray trace). Asterisks indicate truncated action potentials
(APs). D: distribution of latencies of first AP (black bars) and maximum
hyperpolarization (white bars) for cells with onset inhibition. E: first spike
latency (FSL) distribution of VNLL OI neurons. Vertical dashed lines indicate
the average of each sample (see text). Bin widths are 0.25 ms.
Several questions arise from these observations, including
what is the source of this onset inhibition and what is its
function? The short and consistent latency of the IPSPs, its
prominence at noise or tone onset, and its broad frequency
tuning suggest the involvement of the octopus cell pathway.
However, this pathway is excitatory (Adams 1997; Oertel and
Wickesberg 2002), and therefore we hypothesized that this
inhibition resulted from the activation of another VNLL neuron
that received octopus cell inputs (Fig. 2a). For this to be the
case, there must be a subset of VNLL neurons that respond at
short latency and prior to the observed inhibition. Figure 1E
shows that such a cell group exists (n ⫽ 10), responding with
a mean FSL of 4.6 ⫾ 0.3 ms. Importantly, these cells showed
an OI response pattern to contralateral acoustic stimulation
(Fig. 2a1), consistent with an octopus cell input. The proposed
circuitry is also consistent with the anatomical description of
collateral branches from VNLL cells that form local and
presumably inhibitory circuits within this structure (Zhao and
Wu 2001) (Fig. 2, gray axon). Another possible candidate for
the source of this inhibition is the glycinergic principal cell of
the MNTB that is known to project to the VNLL (Glendenning
et al. 1981). However, the narrow frequency tuning and sus-
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The microelectrode was advanced remotely, using a motorized microdrive (MPC-100; Sutter Instruments), in small steps (2 ␮m) once the
VNLL was encountered, but occasionally intracellular recordings
were made from the IC (n ⫽ 14).
Stimuli presented to both ears were 50 ms in duration with 5 ms
rise-fall times and a 500 ms repetition interval; the left and right
transducer outputs were offset by 200 ms. Responsive neurons were
detected using a “search” stimulus of 80 dB noise bursts. Intracellular
impalements were signaled by a sudden and stable drop (⬎25 mV) in
the DC level and the presence of synaptic or large action potentials
(⬎15 mV). Intracellular recordings typically lasted 2 min (maximum:
⬃30 min); however, some recordings lasted for shorter periods, and
only responses to noise bursts were obtained. This limitation was due
to the difficulty in maintaining an in vivo impalement at recording
depths of 5– 8.5 mm from the brain surface. A Maclab 4-s dataacquisition system (AD Instruments, Sydney, Australia) was used to
store membrane potential records (traces) at a bandwidth of 20 or 40
kHz. Once impaled, the neuron’s CF and rate-level function at CF
were determined. Other data (e.g., binaural response properties) were
also sometimes collected as part of a larger study; however, such data
are not presented in this report.
Acoustic stimuli were synthesized digitally and generated by either
Beyer DT48 transducers (Beyerdynamic, Farmingdale, NY) or
Tucker-Davis Technologies (TDT, Gainesville, FL) EC1 electrostatic
speakers in concert with a TDT ED1 speaker driver. All transducers
were controlled by a TDT signal generator (TDT System 2) and
coupled to the end of each hollow earbar. The department’s PC based
“Neurophysiology Laboratory System” (program by R. E. Millard)
was used to control all parameters of acoustic stimulation and data
collection. The acoustic system was calibrated using a Brüel and Kjær
(B&K) measuring amplifier (type 2606, Brüel & Kjær, Naerum,
Denmark). Beyer transducers were calibrated with a B&K 0.5-in
condenser microphone, coupled to a small probe tube positioned
within the ear bar tube ⬃3 mm from the tympanic membrane. The
TDT speakers were calibrated using a 0.25-in B&K condenser microphone inserted into a custom built acoustic coupler designed to
simulate the rat’s ear canal at the end of the hollow earbar (designed
and built by R. E. Millard). Both these methods allowed acoustic input
to be measured in dB sound pressure level (SPL; referenced to 20
␮Pa). The noise bandwidth generated by TDT EC1 speakers was
measured with a Stanford Research Systems dynamic signal analyzer
(SR785, Sunnyvale, CA) and found to be spectrally flat at 80 ⫾ 10 dB
between 20 Hz and 60 kHz. The Beyer transducers had a nominal
bandwidth of 45 Hz to 50 kHz with most of the energy ⬍30 kHz;
there was a gradual roll-off between 5–30 kHz of 10 dB/octave.
Report
POWERFUL, FAST INHIBITION IN THE AUDITORY BRAIN STEM
1653
tained responses of these neurons (Paolini et al. 2001) would
suggest that this is unlikely.
Excluding OI cells, a comparison of cells with and without
(n ⫽ 38) onset inhibition shows that the former group had
longer mean FSLs than the latter group (not shown; respectively, 8.5 vs. 7.3 ms). Therefore this inhibition delays the first
AP in a subset of VNLL neurons. This conclusion is supported
by the data presented in Fig. 2b1; this cell did not exhibit onset
inhibition in a small subset of stimulus presentations (black
traces) and the presence of inhibition (gray traces) resulted in
a longer FSL (means of 6.2 vs. 8.5 ms, respectively).
The amplitude and time course of the fast inhibition described in the preceding text is similar to that observed within
the MNTB, a structure that also receives calyceal inputs
(Awatramani et al. 2004). Awatramani and colleagues (2004)
proposed that fast inhibition may control the excitatory drive
from a calyx. However, in the VNLL the calyx appears to
trigger fast inhibition in a local circuit that produces neural
delays within the VNLL and therefore its output to the IC. The
ramifications of this, and the reason that it occurs in only a
subset of VNLL cells, are unknown but there are several
J Neurophysiol • VOL
possible outcomes at the IC. VNLL neurons receiving onset
inhibition showed either a sustained or onset response to noise
(Fig. 2b, 2 and 3, respectively). The response pattern of these
VNLL neurons will determine the pattern of inhibition in the
IC. Delayed inhibition from VNLL cells with a sustained
response may create phasic responses in the IC (Fig. 2c1),
while delayed inhibition from VNLL onset cells may mediate
pauser IC responses (Fig. 2c2).
The proposed VNLL circuitry predicts the presence of fast
inhibition preceding excitation in the IC (Fig. 2d) because the
inhibitory projection within the VNLL (Fig. 2, gray axon) is a
collateral of an axon projecting to the IC. Note that the VNLL
neuron (Fig. 2b) and the IC neuron (Fig. 2d) receive the same
pattern of inputs, and therefore they would both be expected to
exhibit similar onset inhibition. This prediction is supported by
our intracellular recordings from IC neurons (Fig. 2d1) and
previous reports (Adams 1997; Carney and Yin 1989; Kuwada
et al. 1997; Smith et al. 1993). This inhibitory pathway to the
IC is presumably broadly tuned and would provide a source of
onset-evoked wideband inhibition to narrowly tuned IC neurons (Fig. 2d). In the ventral CN, a similar arrangement exists,
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FIG. 2. Pathways mediating fast inhibition within the VNLL and IC. a: VNLL neuron receiving input from the octopus cell area (OCA) via a thick axon
projection ending in a calyx. a1: intracellular response of a VNLL OI cell. b: VNLL neuron receiving onset inhibition via a collateral (gray) of an ascending axon.
b1:VNLL cell with intermittent onset inhibition. Gray trace, response when inhibition was present; the black trace, response when it was absent. Inset: the average
response (first 15 ms from stimulus onset) with (n ⫽ 3) and without (n ⫽ 7) inhibition. b, 2 and 3: overlayed traces (n ⫽ 20) of onset inhibition in 2 VNLL
cells showing a sustained and onset response, respectively. c: an IC neuron receiving delayed inhibition from a VNLL cell with onset inhibition. c1: an IC neuron
that receives delayed and sustained inhibition from a VNLL cell (as in b2) would be expected to exhibit a phasic response. c2: an IC neuron that receives delayed
and onset inhibition from a VNLL cell (as in b3) would be expected to exhibit a pauser response. Inset: the average response (30 stimulus presentations; first
50 ms from stimulus onset). Pause in AP firing is between 11.7 and 19.4 ms. d: an IC neuron receiving input from a VNLL OI cell (as in a1) would be expected
to show onset inhibition (d1) similar to that observed within the VNLL. Horizontal dashed lines indicate RMPs that were ⫺29, ⫺52, ⫺47, ⫺43, ⫺56, ⫺52, and
⫺26 mV for traces shown in a1, b1– b3, c1, c2, and d1, respectively. Traces shown in a1, b1, c1, c2, and d1 (excluding insets) are responses to a single stimulus
presentation. In all cases, stimuli were 80 dB noise bursts. Inhibitory projections are shaded and excitatory projections are unshaded. Arrows indicate membrane
hyperpolarization. All traces correspond with neurons in the circuit diagram with the equivalent letter.
Report
1654
D.A.X. NAYAGAM, J. C. CLAREY, AND A. G. PAOLINI
is mediated by glycinergic interneurons with onset responses,
and results in the delay of the first AP to off-CF tones (Paolini
et al. 2004). These descriptions of fast, onset inhibition at
several levels of the auditory pathway suggest that it may be a
widespread means of controlling first spike timing.
ACKNOWLEDGMENTS
We thank R. E. Millard for engineering support, A. Xipolitos for technical
assistance, and Prof. G. M. Clark for mentoring and support. These experiments were conducted within the Department of Otolaryngology at The
University of Melbourne.
GRANTS
This work was supported by a Dame Elisabeth Murdoch Scholarship to
D.A.X. Nayagam administered by The Bionic Ear Institute.
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