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J Neurophysiol (November 1, 2002). 10.1152/jn.00119.2002
Submitted on 19 February 2002
Accepted on 1 August 2002
Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Samson, Annie-Hélène and Gerald S. Pollack. Encoding of Sound Localization Cues by an Identified Auditory Interneuron: Effects of Stimulus Temporal Pattern. J. Neurophysiol. 88: 2322-2328, 2002. An important cue for sound localization is binaural comparison of stimulus intensity. Two features of neuronal responses, response strength, i.e., spike count and/or rate, and response latency, vary with stimulus intensity, and binaural comparison of either or both might underlie localization. Previous studies at the receptor-neuron level showed that these response features are affected by the stimulus temporal pattern. When sounds are repeated rapidly, as occurs in many natural sounds, response strength decreases and latency increases, resulting in altered coding of localization cues. In this study we analyze binaural cues for sound localization at the level of an identified pair of interneurons (the left and right AN2) in the cricket auditory system, with emphasis on the effects of stimulus temporal pattern on binaural response differences. AN2 spike count decreases with rapidly repeated stimulation and latency increases. Both effects depend on stimulus intensity. Because of the difference in intensity at the two ears, binaural differences in spike count and latency change as stimulation continues. The binaural difference in spike count decreases, whereas the difference in latency increases. The proportional changes in response strength and in latency are greater at the interneuron level than at the receptor level, suggesting that factors in addition to decrement of receptor responses are involved. Intracellular recordings reveal that a slowly building, long-lasting hyperpolarization is established in AN2. At the same time, the level of depolarization reached during the excitatory postsynaptic potential (EPSP) resulting from each sound stimulus decreases. Neither these effects on membrane potential nor the changes in spiking response are accounted for by contralateral inhibition. Based on comparison of our results with earlier behavioral experiments, it is unlikely that crickets use the binaural difference in latency of AN2 responses as the main cue for determining sound direction, leaving the difference in response strength, i.e., spike count and/or rate, as the most likely candidate.
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Sound localization in the
horizontal plane is based on comparing sounds at the two ears. Sound
arrives earlier at the ear closer to the source, and in general
stimulus intensity is higher at that ear. Some animals can detect the
small (tens of microseconds) binaural difference in arrival time (for
review, see Carr 1993
); others, including insects, rely
mainly on binaural intensity difference as the cue for sound location
(for review, see Pollack 1998).
Two features of the neural response to acoustic stimuli vary with
stimulus intensity: spike count and/or rate increases with increasing
intensity and response latency decreases (Imaizumi and Pollack
2001; Kiang et al. 1965). The binaural
difference in both of these measures varies systematically with sound
location, and either or both might code for sound direction
(Boyan 1979; Eggermont 1998;
Mörchen 1980).
Crickets localize sound both to find mates and to evade predators.
Stridulating male crickets produce songs with relatively low carrier
frequency (dominant frequency for Teleogryllus oceanicus: 4.5 kHz), consisting of repeated trains of sound pulses at rates varying (for T. oceancius) between 8 and 32 pulses/s
(Balakrishnan and Pollack 1996). Echolocating bats
produce ultrasound pulses (20 to >100 kHz), repeated at rates ranging
from a few pulses per second to >100 pulses/s (Griffin et al.
1960). Behavioral experiments have demonstrated that crickets
perform positive phonotaxis (movement toward the sound source) in
response to cricket-like stimuli and negative phonotaxis (movement away
from the sound source) when presented with bat-like sounds
(Moiseff et al. 1978; Nolen and Hoy 1986;
Pollack et al. 1984). The importance of the frequency
ranges of cricket song and bat sounds is reflected by the organization
of the cricket's ear; nearly three-quarters of the approximately 70 receptor neurons in each ear are tuned to cricket-like frequencies, and
more than one-half of the remainder are most sensitive to ultrasonic
frequencies (Imaizumi and Pollack 1999).
When sensory neurons are stimulated with a long series of rapidly
repeated stimuli, their response strength (spike count and/or rate)
decreases for successive stimuli, and response latency increases (Coro et al. 1998; Givois and Pollack
2000; Pasztor 1983). In cricket auditory
receptors, as in mammals (Eggermont and Spoor 1973), the
decline in response strength is greater the higher the sound level
(Givois and Pollack 2000). This implies that neurons ipsilateral to the sound source, where stimulus intensity is higher, will experience a larger response decrement. This may even lead to a
reversal in the sign of the binaural difference in response strength
(contralateral response> ipsilateral; Givois and Pollack 2000). The change in latency of receptor-neuron responses
induced by repeated stimulation does not depend on sound level; thus
directional information encoded by binaural latency difference is not affected.
Phonotaxis responses are not driven directly by receptor neurons, but
rather by interneurons that receive input from receptors. Negative
phonotaxis in response to ultrasound stimuli is initiated by the
identified, bilaterally paired interneuron AN2 (Nolen and Hoy
1984). The effects of the changes in receptor responses
described above might be compensated or exaggerated during signal
transmission from receptors to interneurons, but as yet this issue has
not been studied. In this study, we investigate the effects of rapidly repeated stimulation on encoding of sound localization cues by AN2.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals
Teleogryllus oceanicus were raised in the laboratory on a diet of Purina Cat Chow and water. Unmated females, ages 12-20 days after the final molt, were used in experiments. Crickets were anesthetized by chilling on ice and were mounted on a wax support, ventral side up, after removing their wings and mid- and hind legs. In most experiments, the femur of the fore legs was fixed with a bees' wax-colophonium mixture, parallel to the body axis, and the tibia and tarsus were held flexed against the femur, simulating their position during flight. When recordings were made from receptor neurons, the legs were rotated around the coxa-trochanter-femur joints so as to project perpendicularly from the body axis, exposing the anterior surface of the femur for electrode implantation (see Electrophysiology).
Electrophysiology
For extracellular recordings of AN2, the cervical connectives
were exposed and placed on a pair of silver-wire hook electrodes. AN2
produces the largest sound-evoked spikes in the cervical connectives, and these are easily recognized by visual inspection (Moiseff and Hoy 1983, see inset of Fig.
1A). To record compound action potentials of auditory receptor neurons, we inserted a Teflon-coated silver wire (114 µm OD) into the anterio-dorsal surface of the femur,
close to the nerve branch carrying the axons of the receptor neurons
from their origin in the prothoracic tibia to the prothoracic ganglion.
The indifferent electrode was placed proximally and ventrally in the
femur (see Pollack and Faulkes 1998 for further details). For intracellular recordings of AN2, the prothoracic ganglion
was exposed and supported on a metal platform. The ganglion was
submerged in physiological saline (Strausfeld et al.
1983) and recordings were made using microelectrodes (>30
M
) filled with 2 M K acetate. Electrophysiological recordings were
digitized (Digidata 1320A, 10 kHz sampling rate, Axon Instruments)
using the program AxoScope 8.0 (Axon Instruments). Responses were
viewed and analyzed using custom-written programs (GP) for Scilab
(www-rocq.inria.fr/scilab/), and statistical analysis were performed
using Statistica for Windows (StatSoft, Tulsa, OK).
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Stimuli
Stimuli consisted of trains of trapezoid-shaped sound pulses of
30-ms duration, including 5-ms rise and fall times. Carrier frequency
was 30 kHz, which is within the range of AN2's greatest sensitivity
(Moiseff and Hoy 1983). Pulse trains were 30-45 s long
and were preceded by 60 s of silence. Pulses were presented at
rates of 0.3, 8, 16, and 26 pulses/s (pps). The lowest pulse rate was
presented at the beginning, middle, and end of each experiment, and
responses were statistically indistinguishable in all cases. This
ensured both that responsiveness remained stable, and that the 60-s
pause following each stimulus was sufficient for return to baseline
responsiveness. The order of presentation of stimuli varied from
experiment to experiment, with the two highest pulse rates most often
presented in the middle of the series. Stimuli were produced, using
LabWindows programs (National Instruments), by a D/A circuit
(ATMIO16F5, National Instruments, Austin; D/A update rate 200 kHz) and
were attenuated (PA4, Tucker-Davis, Gainesville, FL), amplified (D150A,
Amcron, Elkhart, IN), and broadcast through loudspeakers (RadioShack,
40-1310B) situated on the cricket's left and right in the horizontal
plane, perpendicular to the longitudinal axis, at a distance of 50 cm.
The loudspeakers and cricket were housed in a chamber lined with
echo-suppressing mineral-wool wedges. Sound pressure level in dB re
2 × 10
5 Nm2 (SPL)
was measured at the cricket's position with a Brüjel and Kjaer
(Naerum, Denmark) 4135 microphone and 2610 measuring amplifier.
Data analysis
The response to each sound pulse was analyzed over a time window
that included the entire response as determined by visual inspection.
Time windows for AN2 responses ranged from 38 ms (26 pps) to 50 ms (0.3 pps) in duration and were constant for each pulse rate across
experiments; for receptor responses, windows ranged from 24-26 ms, and
were constant for all measurements in an individual cricket. Measuring
AN2 spike count and latency was straightforward, because each
individual spike could clearly be detected (e.g., Fig. 1A,
inset). For receptor neurons, response strength was
quantified by integrating the recording over the response time window,
following high-pass filtering (100 Hz) and full-wave rectification.
Receptor response latency was taken as the time, relative to stimulus
onset, of the first negative peak of the compound action potential
revealed by signal averaging (see inset, Fig.
4B); this peak represents the nearly synchronous firing of
many receptors neurons. See Givois and Pollack (2000) and Pollack and Faulkes (1998) for further details.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Effects of repeated stimulation on spike count and first-spike latency
Responses of AN2 to stimuli presented at low repetition rate are stable, both in spike count and in latency (Fig. 1, 0.3 pps). With more rapid stimulation, responses change systematically through time. An initial very rapid decrement in spike count is followed by a slower asymptotic decline that last for several seconds (Fig. 1A). Short and long time constants, derived from double-exponential curve fits (see Fig. 1 legend), were 303 ± 266 ms and 11.71 ± 8.18 s (mean ± SD; pooled data for 70 and 90 dB, and 8, 16, and 26 pps, averaged from 7 crickets). Neither time constant varied with either sound level or pulse rate (ANOVA, P values range from 0.27 to 0.36).
First-spike latencies lengthen with repeated stimulation (Fig.
1B) and also show rapid and slower phases of increase (time constants: 1.39 ± 0.64 ms; 47.87 ± 15.72 s). Note that the
variability of latency decreases significantly with intensity (mean
variance for 7 crickets, of responses between 8 and 10 s after
stimulus onset is 4.37 ms, at 90 dB; 17.32 ms at 70 dB;
F6 = 6.9, P = 0.01; we
focus on the interval 8-10 s after stimulus onset to facilitate comparison of our results with earlier behavioral experiments; Pollack and El-Feghaly 1993; see
DISCUSSION). In addition, variability of latency increases
as the train of stimuli continues with larger increases at lower
intensities and higher pulse rates (ANOVA on mean variance of responses
between 8-10 s after stimulus onset: pulse-rate effect,
F6 = 23.9, P < 0.001, intensity effect, F6 = 13.2, P < 0.001). Variability of spike count is similar for the range of pulse rates and intensities examined (ANOVA; pulse-rate effect, P = 0.4; intensity effect, P = 0.5).
Effects of intensity and pulse rate on changes in spike count and latency
Figure 2A summarizes the decremented response as the mean of responses to sound pulses delivered between 8 and 10 s after stimulus onset. As expected, the number of AN2 spikes/sound pulse increases with intensity. However, because of the pulse-rate-dependent response decrement, the increase is less pronounced the higher the pulse rate.
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The increase in latency with repeated stimulation (Fig. 1B) also depends on both pulse rate and intensity. The higher the pulse rate, and the lower the intensity, the greater the increase in latency (Fig. 2B).
Therefore the effects of repeated stimulation on spike count and on first-spike latency vary with both intensity and pulse rate. The effect of pulse rate is similar for both response parameters: higher pulse rates produce larger response changes. The effect of intensity, however, differs: at higher intensities, the decrease in spike count is more pronounced, but the change in latency is less pronounced.
Effects of repeated stimulation on localization cues
The stimulus intensity of a 30-kHz sound may be 
15-20 dB higher
at the ipsilateral than at the contralateral ear (Wyttenbach and
Hoy 1999; personal observations). This, together with the intensity dependence of the response changes described above, implies
that the changes in response resulting from repeated stimulation may
alter binaural differences. Figure 3
shows binaural differences measured from simultaneous recordings of the
left and right AN2. Rapidly repeated stimulation results in a decrease
in the binaural difference in spike count, but an increase in the
binaural latency difference. The change in spike-count difference is
monotonic with pulse rate, whereas the latency difference reaches a
maximum at 16 pps.
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Response decrement is greater in interneuron AN2 than in receptor neurons
It seems probable that, as for low-frequency receptors
(Givois and Pollack 2000), responses of ultrasound
receptors decline with repeated stimulation (Coro et al.
1998). If so, then the effects we describe for AN2 might be
accounted for simply by response decrement of receptor neurons. To
determine whether this is the case, we compared the decrement of
compound action potentials recorded from the whole auditory nerve with
the decrement of AN2 responses. Ultrasound receptors comprise only a
small proportion of the entire receptor population (Imaizumi and
Pollack 1999), and as a result, clear whole-nerve responses,
which reflect synchronous activity of many receptors (Pollack
and Faulkes 1998), can be recorded reliably only for high
stimulus levels late in the pulse train, by which time responses have
decremented. For this reason, we compare responses of AN2 and receptors
only for high stimulus levels (90-100 dB). To compare AN2 response
strength (spike-count) to the auditory response (integrated whole-nerve
recording, see METHODS), we normalized the decremented
responses with respect to the mean response to a low-pulse-rate
stimulus (0.3 pps) at the same intensity; as shown in Fig.
1A, stimulation at this repetition rate does not induce
response decrement. As shown in Fig. 4,
response decrement is more severe for AN2 than for the auditory
receptors. In addition, the effects of pulse rate on response decrement
and change in latency are stronger for AN2 than for receptors [2-way ANOVA: interaction effect between pulse rate and level of measurement (receptor or AN2) on relative response magnitude:
F(3,62) = 86.27, P < 0.0001; on
latency: F(3,62) = 14.59, P < 0.0001].
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Changes in membrane potential
The observation that response decrement of AN2 is more pronounced than that of receptors suggests that factors in addition to decremented receptor responses may also be involved. We examined this possibility by recording from AN2 intracellularly.
During the course of stimulation, a slowly building, long-lasting hyperpolarization builds up in AN2. This is most clearly evident as a strong hyperpolarization following the termination of stimulation, shown in Fig. 5A. An additional indication is the decrease in membrane potential reached between sound pulses, shown in Fig. 5, B (thin arrow) and C.
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A known source of inhibition of AN2 is the interneuron ON1 which is
excited by input from the contralateral ear (Faulkes and Pollack
2000; Selverston et al. 1985). Following removal
of the contralateral ear, both the decrease in membrane potential
between successive responses (Fig. 5C) and the inhibition
following the termination of stimulation (data not shown) were still
present. Cutting the contralateral leg nerve, which includes the axons of auditory receptors, affected neither the decline of AN2's spike count, nor the increase in latency (Fig. 5D). Thus neither
the hyperpolarization of AN2, nor the decrement in AN2's spiking
response with repeated stimulation, are due to contralateral inhibition.
In parallel with the build-up of hyperpolarization in AN2, the level of depolarization reached during successive excitatory postsynaptic potentials (EPSPs) decreases [Fig. 5, B (thick arrow) and C). Like the decrement in spike count, the membrane potential at the peak of the EPSP, during the period 8-10 s after stimulus onset (thick arrow in Fig. 5B), varies with pulse rate and intensity (Fig. 5E). The decrease in EPSP amplitude likely reflects a combination of factors, including decrement of receptor responses (Fig. 4), shunting of excitatory current through channels responsible for the slow hyperpolarization, and perhaps depression of receptor-to-AN2 synaptic transmission as well.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Our results show that ultrasound localization cues encoded by AN2 are affected by rapidly repeated stimulation. The spiking response decreases with time (Fig. 1), and this change is more pronounced at higher intensity and pulse rate (Fig. 2). First-spike latency increases with time and, as for the change in spike count, the increase in latency is greatest for high pulse rates. However, the effect of intensity is opposite to that on spike count; the change in latency decreases with increasing intensity (Fig. 2).
The intensity dependence of these response features is of particular importance when considering binaural cues used in sound localization. The decrement in AN2's spiking response is greater for the neuron ipsilateral to the sound source, and as a result, the binaural difference in spike count decreases. In contrast, because the change in latency with repeated stimulation is smaller at higher intensities, the binaural difference in response latency increases as stimulation continues.
The larger latency shift at lower intensities may be due to the shape
of the relationship between latency and stimulus intensity. For AN2, as
for most interneurons, latency decreases asymptotically as stimulus
intensity increases (Moiseff and Hoy 1983), presumably because the rate of rise of the EPSP increases to a maximum (perhaps set by membrane biophysics) as excitatory input increases.
Consequently, intensity changes have a larger effect on latency at the
low end of the intensity range. Excitatory input to AN2 decreases
during repeated stimulation, in part because of decrementing responses of receptor neurons (Fig. 4), and possibly also because of synaptic depression. The decrease in excitation should be functionally equivalent to a decrease in stimulus intensity. This decrease, occurring at an already low stimulus intensity, can be expected to
produce a large shift in latency. Consistent with this interpretation, our intracellular recordings show that the rise time of the EPSP increases for successive stimuli, particularly for lower stimulus intensities (data not shown).
Our intracellular recordings show that in addition to decreasing
excitatory input, a hyperpolarizing current may also play a role in
AN2's response decrement. Two sources of inhibitory synaptic input to
AN2 have been described previously: 1) contralateral inhibition, originating in the contralateral identified neuron ON1
(Faulkes and Pollack 2000; Selverston et al.
1985), and 2) ipsilaterally derived inhibition of
unknown origin (Moiseff and Hoy 1983). The
hyperpolarization persists after removing the contralateral ear (Fig.
5C); thus it is either ipsilateral in origin and/or intrinsic to AN2. The ipsilateral inhibition described by
Moiseff and Hoy (1983) is recruited most effectively by
low-carrier-frequency stimuli. However, some low-frequency-tuned
receptor neurons are stimulated by intense ultrasound (Imaizumi
and Pollack 1999); thus we cannot rule out this source. Slowly
building, long-lasting hyperpolarization similar in time course to that
which we observed in AN2 has been described in other auditory neurons
of insects (Pollack 1988; Römer and Krusch
2000). In the ON1 neuron of Acheta domesticus, this
hyperpolarization is triggered by activity-associated Ca2+ accumulation (Sobel and Tank
1994).
The presumed function of negative phonotaxis in crickets is bat evasion
(Hoy 1992). Bat echolocation sounds span a broad range of temporal patterns, varying both with the species of bat and with the
progression of the bat-insect interaction (Griffin et al.
1965). Before a bat has encountered a potential prey, during the "search" phase of echolocation, echolocation cries are emitted over roughly the same range of pulse rates as in our experiments (6-35
pps) (Jones 1999). During the "terminal" phase, just
before capture, pulse rate may exceed 100/s (Griffin et al.
1960). Pulse durations of echolocation sounds are generally
shorter than the 30-ms sounds we used (which we chose to facilitate
comparisons with earlier behavioral work), and it seems reasonable to
suppose that pulse duration might affect the extent of response
decrement. However pulse durations of several to tens of milliseconds
are typical of high-duty-cycle bats (Jones 1999).
Northern Australia, where T. oceanicus live (Hill et
al. 1972), is home to at least five species of Hipposidaridae
(Hoffmann et al. 1982), a subfamily characterized by
high-duty-cycle calls (Jones 1999). Thus it is plausible
that T. oceanicus might be exposed, in nature, to bat cries
that would induce considerable decrement of AN2 responses.
Habituation of ultrasound-induced behavioral responses of T. oceanicus has been studied in the laboratory (Engel and Hoy
1999; May and Hoy 1991). These studies showed
that negative phonotactic responses declined when crickets were
stimulated with pulses (either 10 or 50 ms in duration) presented at
rates of 1.3 pps and 2/s. We saw no decrement in the response of AN2
when 30-ms pulses were presented at a rate of 0.3/s, and considerable
decrement when the pulse rate was 8/s. Unfortunately, we have no data
on AN2's response to the pulse rates used in the habituation studies,
so we cannot say to what extent the decline in AN2 response might contribute to behavioral habituation. May and Hoy (1991)
suggest that behavioral habituation is not the result of declining AN2 responses, based on an earlier physiological study of AN2 (Nolen and Hoy 1987) that, they claim, failed to find significant
response decrement even at a pulse rate of 15/s. Our results are
clearly at odds with this. However, the data on which the claim for
lack of decrement in AN2 is apparently based, Fig. 12 of Nolen
and Hoy (1987), show a substantial decline in AN2's response,
from approximately 12 spikes to the first sound pulse to 7 spikes to the second. Nevertheless, the phenomenology of AN2's response decrement and behavioral habituation do differ, suggesting that habituation is not accounted for entirely by AN2's response decrement. In particular, behavioral habituation is greatest at low stimulus intensities (May and Hoy 1991), whereas the decline in
AN2's response is most pronounced at high intensities (Fig. 2).
It is unclear to what extent the decrement in AN2's response might
affect natural behavior. The initial response to ultrasound, at lower
intensities, is a short-latency turn away from the sound source, and it
is possible that this would remove the cricket from the sound field of
the bat's echolocation cry before substantial response decrement could
occur (cf. Miller 1983). When stimulated with
higher-intensity ultrasound, crickets react in a nondirectional manner
(Nolen and Hoy 1986), so the effects of response
decrement on sound localization cues might be irrelevant. Estimating
the degree to which stimulus-induced changes in localization cues might
play a role in bat-cricket interactions must await field observations,
which are currently lacking.
No matter what its relevance to natural behavior, the decrement we
describe, when compared with earlier laboratory experiments, helps to
illuminate how ultrasound location is represented at the level of the
AN2 neurons. Pollack and El-Feghaly (1993) described the
effects of pulse rate on phonotactic responses of T. oceanicus to ultrasound stimuli. Their stimuli, like ours,
consisted of trains of 30-ms duration sound pulses, with pulse rates
ranging from 8 to 32 pulses/s. Presumably, binaural difference in spike count and latency of AN2, and in particular their changes throughout the course of the pulse trains, were similar in their experiments to
that which we describe. Pollack and El-Feghaly found that the initial
phonotaxis response to stimulation was reliably directed away from the
sound source for all pulse rates tested. However, at high pulse rates,
i.e., under conditions that produce the largest changes in response of
AN2, these initial, negative, responses were transient (approximately
1 s in duration), and by 10 s after the onset of stimulation,
phonotaxis was on average toward, rather than away from, the sound
source. Our physiological results show that the binaural difference in
response latency after 10 s of stimulation is larger than that at
stimulus onset, suggesting that if the crickets relied mainly on
latency difference as the cue for sound direction, their behavioral
responses should not have reversed in direction. By contrast, the
binaural difference in spike count, which initially strongly favors the
ipsilateral AN2, is near zero after 10 s of stimulation. It seems
likely, then, that the reversal in behavioral response direction is due in part to the loss of directional information encoded as binaural spike-count difference. It is unclear, however, why the response reverses in direction, rather than simply disappearing. Nevertheless, comparison of our physiological results with these earlier behavioral studies suggests strongly that binaural latency difference is not the
chief cue for determining sound direction. This agrees with recent
experiments that indicate that the same may be true for localization of
cricket song (Pollack 2001), but contrasts with a recent
model of phonotaxis in crickets, in which latency difference is the
pertinent cue (Webb and Scutt 2000).
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ACKNOWLEDGMENTS |
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This work was supported by the Natural Science and Engineering Research Council of Canada.
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FOOTNOTES |
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Address for reprint requests: G. S. Pollack, Dept. of Biology, McGill University, 1205 Ave. Doctor Penfield, Montreal, Quebec H3A 1B1, Canada (E-mail: gerald.pollack{at}mcgill.ca).
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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