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IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 47, NO.

3, MARCH 2000 389

Nonlinear Adaptive Filtering of Stimulus Artifact


Richard Grieve, Philip A. Parker*, Senior Member, IEEE, Bernard Hudgins, Member, IEEE, and
Kevin Englehart, Member, IEEE

Abstract—Noninvasive measurements of somatosensory evoked distortion of the SEP, [4]. Fourth, the mechanisms by which
potentials have both clinical and research applications. The elec- the electrical stimulus is coupled into the recording are varied,
trical artifact which results from the stimulus is an interference complex and distributed, making minimization of the SA at the
which can distort the evoked signal, and introduce errors in
response onset timing estimation. Given that this interference is source problematic [5].
synchronous with the evoked signal, it cannot be reduced by the Given that the conventional methods are not effective for SA
conventional technique of ensemble averaging. The technique of reduction in SEP measurements, alternative approaches have to
adaptive noise cancelling has potential in this regard however, and be considered. A technique which has potential in this regard
has been used effectively in other similar problems. An adaptive is adaptive noise cancelling (ANC). In this approach an esti-
noise cancelling filter which uses a neural network as the adaptive
element is investigated in this application. The filter is imple- mate of the SA is obtained via an adaptive filter and the esti-
mented and performance determined in the cancelling of artifact mate subtracted from the composite SA plus SEP signal. ANC
for in vivo measurements on the median nerve. A technique of filters have been used in other biological signal acquisition ap-
segmented neural network training is proposed in which the plications. Ye and Choy [6] used such a filter for the reduction of
network is trained on that segment of the record time window respiratory artifact in rheopneumography measurements. Sada-
which does not contain the evoked signal. The neural network is
found to generalize well from this training to include the segment sivan and Narayana [7] developed an ANC filter for the reduc-
of the window containing the evoked signal. Both quantitative tion of electrooculogram in electroencephalography measure-
and qualitative measures show that significant stimulus artifact ments. Thakor and Zhu [8] have used an ANC filter for the re-
reduction is achieved. moval of the QRS complex in ECG in order to improve detec-
Index Terms—Adaptive, artifact, cancelling, evoked, filter, re- tion of the -wave. Suzuki et al. [9] developed a real-time ANC
sponse, stimulus. filter for suppression of ambient noise in lung sound measure-
ments.
I. INTRODUCTION In the application of noise cancelling to SA reduction,
McGill et al. [4] estimated the artifact waveform from sub-

S OMATOSENSORY evoked potentials (SEP’s) are used


widely in clinical and research applications, and include
peripheral, spinal, and cortical potentials. For reasons of
threshold stimulation and subtracted the estimate from the
suprathreshold stimulus response. Nonlinear adaptive ANC
filters were not considered in this study. Work by one of the
convenience, comfort, and safety, the preferred measurement present authors investigated the application and performance
techniques are noninvasive using surface electrical stimulation of linear and nonlinear finite impulse response (FIR) ANC
and recording electrodes. The recorded SEP is thus small in filters for SA reduction in SEP measurements [10], [11]. The
amplitude—typically on the order of a microvolt peak [1]. performance of linear FIR ANC filters was found to be rather
While an electrical stimulus evokes the desired response from poor [10] suggesting that the input–output relationship of tissue
the nervous process of interest, it also results in an interfering to electrical stimulus is nonlinear. Indeed the source of this
potential referred to as the stimulus artifact (SA). nonlinearity is, at least in part, the nonlinear voltage–current
Due to a number of factors, the stimulus artifact is a partic- characteristic of the skin [12]. A second-order truncated
ularly troublesome form of interference. First, the amplitude of Volterra series nonlinear FIR ANC filter was shown to have
the SA is typically orders of magnitude larger than the SEP, [2]. substantially improved performance [10].
Second, the SA is synchronous or coherent with the SEP and While this filter achieves good SA cancellation, it has two
thus cannot be reduced by ensemble averaging—the common serious limitations: 1) it cannot model nonlinearities of order
method for reducing other forms of interference, [3]. Third, in higher than two and 2) the number of filter coefficients grows
most cases the SA overlaps the SEP in both the time and fre- as the square of the FIR filter length. An alternative ANC filter
quency domains, such that conventional time windowing and that does not suffer from these limitations is the neural network
frequency filtering are not capable of removing the SA without (NN) configuration. The objectives of this paper are to investi-
gate the application and performance of the NN ANC filter for
Manuscript received September 11, 1998; revised October 8, 1999. This work the reduction of SA in SEP measurement.
was supported in part by the NSERC under a Postgraduate Scholarship and
Grant OGP0004445. Asterisk indicates corresponding author.
R. Grieve B. Hudgins, and K. Englehart are with the Department of Electrical II. NN ANC FILTER
and Computer Engineering and Institute of Biomedical Engineering, University
of New Brunswick, Fredericton, NB, E3B5A3 Canada. The NN configuration has been used in ANC filters for other
*P. A. Parker is with the Department of Electrical and Computer Engineering applications requiring cancellation of different types of interfer-
and Institute of Biomedical Engineering, University of New Brunswick, Fred-
ericton, NB, E3B5A3, Canada (e-mail: pap@unb.ca). ence. Yuwaraj et al. [13] applied the NN ANC filter for cancel-
Publisher Item Identifier S 0018-9294(00)01772-9. lation of interference in otoacoustic emission measurements. In
0018–9249/00$10.00 © 2000 IEEE
390 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 47, NO. 3, MARCH 2000

associated weights, , are included in practice in order to


accommodate dc offsets.
During the training phase, the NN weights are updated, from
small randomly selected initial values, using the back-propaga-
tion algorithm [15]. The update equations are given by

and

Fig. 1. Adaptive noise cancelling (AN) filter structure.


where
is the time index;
is the learning rates for layer 1;
is the learning rate for layer 2;
is the derivative of the activation function evaluated at
;
is the cancellation error at time index .
Appropriate values for , and are determined by per-
formance and stability criteria to be considered in Section IV as
part of two in vivo experiments.
These experiments require the acquisition of SEP and SA
data, and Section III describes the acquisition methodology.

III. METHODOLOGY
A block diagram of the measurement system for acquiring
Fig. 2. Feedforward neural network structure.
SEP from the median nerve is shown in Fig. 3. Median nerve
sensory fibers are stimulated at the finger and SEP acquired at
the wrist using surface Ag/AgCl electrodes. The resulting SEP
the first application to SA reduction, Grieve et al. [14] inves- and SA are amplified over the bandwidth 10 Hz to 10 kHz,
tigated the pi–sigma NN configuration with some success but sampled at a rate of 25.6 kHz, and the digital data stored for
concluded that a feedforward NN configuration would be more subsequent off-line processing. Following each stimulus, a data
appropriate. The feedforward multilayer perceptron (MLP) NN window of 10 ms or 256 samples is recorded. The Bruel and
will be considered in this paper for the ANC filter and SA can- Kjaer 2032 signal analyzer is used in an on-line ensemble aver-
cellation. aging mode in order to confirm the presence of SEP during the
The general configuration for the ANC filter is given in Fig. 1. recording session. In order to ensure no SEP crosstalk between
The primary channel input is the addition of evoked re- the primary and reference inputs to the ANC filter, a necessary
sponse , artifact , and uncorrelated noise . The reference condition for an ANC filter, a double-stimulus single-channel
channel input is the addition of artifact , correlated with technique is used. In this technique a series of alternating sub
through the system , and uncorrelated noise . The adap- and supra threshold stimuli are applied to the finger. The re-
tive filter estimates from and is adapted by the error sponses to the subthreshold stimuli are used as the reference
through an appropriate training algorithm. Following conver- data, and those to the suprathreshold as the primary data. Thus
gence of , the ANC filter output is the minimum mean no channel crosstalk is possible. This technique also has the ad-
square error estimate of . vantage of requiring only a single data acquisition channel and
Different structures can be used for the adaptive filter, associated hardware.
, and perhaps the most common is the linear FIR filter. Two Grass S11 stimulators with isolators are used to generate
However the structure of interest here is the NN adaptive the series of stimuli. Fig. 4 shows a typical series of stimuli and
filter because of its ability to generalize from training to test acquired data for this technique.
data, and to model nonlinear transfer functions of arbitrary
order. The general structure of a feedforward MLP neural
IV. EXPERIMENT 1
network is given in Fig. 2. For the implementation in this
paper, samples, , from form the In order to optimize the NN parameters and evaluate the NN
-dimensional input feature vector for the input layer. The ANC performance, the first experiment acquired data without
input layer is fully connected to the hidden layer through the the presence of SEP. In this way the cancellation performance
weights , where is the number of can be examined over the full SA duration, including the time
hidden nodes. The hidden layer is connected to the output layer interval in which the SA would otherwise overlap the SEP. If the
through the weights , and hyperbolic SEP were present and unknown it would be impossible to pre-
tangents are used for activation functions. The bias inputs and cisely evaluate the filter’s performance in cancelling the SA. At
GRIEVE et al.: NONLINEAR ADAPTIVE FILTERING OF STIMULUS ARTIFACT 391

Fig. 3. Stimulation and acquisition system.

Fig. 4. (a) Alternating sub and supra electrical stimuli and (b) resulting SA and SEP.

the same time the network parameters can be studied and op- training, the record time windows were divided into two seg-
timized—in particular network size and training data window ments, and , such that segment contains no SEP and ,
will be investigated. The methodology of Section III was used to which is the remainder, contains the SEP. This training method
collect 300 primary and reference records. However, for this ex- is referred to as segmented-training. Fig. 5 shows an example of
periment both reference and primary stimuli were subthreshold, the segments and . Due to the finite conduction velocity of
thus ensuring no SEP in either channel. the nerve fiber, there is always a time delay between the stimulus
Because the SA and SEP are correlated, it is essential to application and the onset of the SEP. This interval determines
ensure that during NN training with SEP present, the primary the magnitude of the time segment . The value of for prac-
channel training data not contain SEP. Otherwise the NN filter tical application can thus be based on the minimum expected
will adapt to cancel not only SA but also the SEP. Thus for nerve conduction delay between stimulus and SEP arrival at the
392 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 47, NO. 3, MARCH 2000

the AN filter performance. Thus the performance measure is


of particular significance.
The 300 acquired response records were divided randomly
into a 150-record training set and a 150-record test set. The pri-
mary and reference inputs used to train the NN were generated
by averaging the training set data. These inputs were made up
of the first 40 data points, preceded by a 20 point zero pad.
The training was continued until the incremental change in the
mean squared error with each iteration was not significant, indi-
cating convergence of the network. The NN size was optimized
by varying the number of input and hidden nodes, training the
network for each combination, and determining the values of
, and for the test set. The number of input and hidden
nodes were varied over 4–20, and 2–14, respectively. Data were
collected and processed for six subjects, and the results for one,
which is typical of the 6, are shown in Fig. 6. After considering
the results for all subjects, and keeping in mind that is of
particular importance here, the combination of 12 input nodes
and six hidden nodes was selected as optimum for further im-
plementations. The low value is due to the fact that the SA
power in of the primary channel is comparable to the uncor-
Fig. 5. The P and P segments for segmented training. The filter is trained on related channel noise power, hence limiting the maximum value
the P segment where no SEP is present.
that can attain.
To determine the generalization ability of the filter, the length
recording electrodes. For the median nerve and this measure- of the training section was varied over 20–100 data points from
ment setup, a value of 40 samples or 1.56 ms is appropriate. In a record length of 256 points, the NN trained, and the perfor-
other applications an appropriate value can always be esti- mance measure calculated . The results are shown
mated. It is important that this estimation and segmentation be in Fig. 7. Again is the measure of most significance since it
carefully done as the algorithm training is sensitive to the par- measures the performance in , and hence the ability of the NN
titioning—if the segment is too short poor generalization of to generalize. The value of is fairly constant over the training
the filter will result and if too long some cancellation of the SEP range tested indicating that the NN is generalizing well (this ob-
can occur. servation will be considered in more detail in Section VI). Also
The performance measures for the AN filter relate to residual shown in Fig. 7 is the performance of a nonlinear FIR AN filter
SA in the filter output as a ratio to the SA in the primary channel. with 10 taps [10] trained with the recursive least squares algo-
Specifically the measures are , and as defined by rithm, (NRLS), and operating on the same data. For this filter,
generally continues to increase with indicating that its gen-
eralizing ability is not as strong as the NN for in the range
necessary for practical application, i.e., in this case.
and
V. EXPERIMENT 2
In this experiment the NN ANC filter of Section IV was used
where to cancel SA in SA plus SEP signal from six subjects. The
is the SA component at time-index in the pri- methodology of Section III, using both sub and supra threshold
mary; stimuli as per Fig. 4, was used to acquire the data. As in Sec-
is the SA component at time-index in the output; tion IV, 300 primary and reference records were acquired, and
is the standard deviation of the random variable ; these were randomly split into a 150-record training set and a
is a time segment of the record window; 150-record test set. In order to test the practical effectiveness of
is a time segment containing the remainder of the the filters, the final outputs were obtained by filtering each of
record window; the 150 records in the test set, and averaging the 150 results.
is a measure of the reduction of the SA peak; The primary and reference inputs used to train the NN were
is the measure of the power reduction of the SA in generated by averaging the training set data. These inputs were
segment ; made up of the first 40 data points, preceded by a 20 point zero
is the measure of the power reduction of the SA in pad. The training was continued until the incremental change
segment . in the mean squared error with each iteration was not signifi-
Since the NN was trained on the segment , which contains cant, indicating convergence of the network. The resulting filter
only a portion of the SA, the ability of the NN to generalize and was then used to filter the 150 records in the test set, and the
accurately generate from in both and is critical to 150-record filter output was averaged to obtain the final output.
GRIEVE et al.: NONLINEAR ADAPTIVE FILTERING OF STIMULUS ARTIFACT 393

Fig. 6. Network size test on subthreshold stimulus data showing performance as a function of the number of input and hidden nodes.

the filter, the output contains a very high residual interference.


To prevent the NRLS filter from converging on large kernel
values, it was trained on raw data, rather than averaged data. All
150 primary and reference pairs in the training set were used
to train the filter. Each record was composed of a 20 point zero
pad followed by 40 points of data. The resulting filter was then
used to filter the 150 records in the test set, and the 150-record
filter output was averaged to obtain the final output. It should
be noted that the performance measure cannot be used in this
experiment. Since the SEP is present and unknown, the residual
SA following cancellation cannot be evaluated quantitatively.
Therefore performance evaluation in the segment must be
a qualitative observation of the SA reduction in the overlap re-
gion, relative to the SEP.
Fig. 7. Performance  versus length of training segment.
Table I gives and values for the two adaptive filters,
NN and NRLS FIR, used in the AN filter over the six subjects.
The training of the NRLS filter was slightly different. It was It is evident that both give substantial reductions in the SA over
found that when the NRLS filter is trained on averaged data, the the segment . It is also evident that the NN gives a somewhat
kernel values upon which it converges are large numbers. If a larger reduction which is to be expected given that the NRLS is
signal is filtered that is slightly different than that used to train able to model second order nonlinearities only while the NN can
394 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 47, NO. 3, MARCH 2000

TABLE I 35 dB averaged over six subjects. Since the NN can model a


PERFORMANCE MEASURES  AND  FOR
nonlinearity of arbitrary order it was able to achieve a larger
EXPERIMENT 2 OVER SIX SUBJECTS
reduction than an NRLS FIR AN filter based on the truncated
second order Volterra model. It was also demonstrated that the
NN is able to provide better generalization from the to the
segments. The SA cancellation in the interval was shown
qualitatively to be excellent.
Fig. 7 demonstrates the power of the NN in generalizing, and
identifying/modeling the nonlinear system between the primary
and reference channels. The fact that is relatively constant
over the length of investigated indicates that it is able to cap-
ture and model the nonlinear system well with as few as 20
samples per evoked response. For this reason, the NN AN filter
trained in the segment is able to provide excellent SA can-
cellation in the segment. In contrast, the NRLS AN filter
requires a of approximately 70 samples to achieve the same
performance, by which time the SA is typically overlapping the
SEP. The difference is no doubt due to the second order nonlin-
earity modeling limitation of the NRLS, as well as the structural
differences in the NN and FIR adaptive filters. The dip in seen
for both filters as increases is likely due to the fact that in the
early part of the SA is very large compared to the uncorre-
lated noise, and hence the adaption converges well. However
in the later part of the SA falls rapidly to values comparable
to the uncorrelated noise and the adaption and convergence are
disturbed. A corresponding drop in performance occurs until
is sufficiently large to allow the adaption to recover.
From the results of Table I and the small residual SA of Fig. 8,
it is clear that the NN adaptive filter has converged well and
has identified/modeled the nonlinear system well. When
considering training and convergence times, it is noted that in
the case where the SA is stationary, the NN can be trained, the
coefficients fixed, and SEP measurements made on-line or off-
line. In the case of nonstationary SA, the NN adaptive filter can
be allowed to track SA changes over time by using appropriate
values for and in the update algorithm, [11]. Tracking
and convergence properties of the filter in this mode need to be
investigated further in a continuation of this work.
Fig. 8. SA cancellation results from Experiment 2 for subjects a; b, and c.

REFERENCES
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tortion and onset timing errors. An ANC filter with a NN as tive FIR filters in rheopneumographic measurements,” Med. Biol. Eng.
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[8] N. V. Thakor and Y. S. Shu, “ Applications of adaptive filtering to ECG Philip A. Parker (S’70–M’73–SM’86) received the
analysis: Noise cancellation and arrhythmia detection,” IEEE Trans B.Sc. degree in electrical engineering from the Uni-
Biomed. Eng., vol. 38, pp. 785–793, Aug. 1991. versity of New Brunswick (UNB), Fredericton, NB,
[9] A. Suzuki, C. Sumi, K. Nakayama, and M. Mori, “Real-time adaptive Canada, in 1964, the M.Sc. degree from the Univer-
cancelling of ambient noise in lung sound measurements,” Med. Biol. sity of St. Andrews, St. Andrews, U.K., in 1966, and
Eng. Comput., vol. 33, pp. 704–708, 1995. the Ph.D. degree from the UNB in 1975.
[10] V. Parsa, P. A. Parker, and R. N. Scott, “Adaptive stimulus artifact re- In 1996, he joined the National Research Council
duction in noncortical somatosensory evoked potential studies,” IEEE of Canada as a Communications Officer and the fol-
Trans. Biomed. Eng., vol. 45, pp. 165–179, Feb. 1998. lowing year he joined the Institute of Biomedical En-
[11] , “Convergence characteristics of two algorithms in nonlinear stim- gineering, UNB, as a Research Associate. In 1976, he
ulus artifact cancellation for electrically evoked potential enhancement,” was appointed to the Department of Electrical Engi-
Med. Biol. Eng. Comput., vol. 36, pp. 1–13, 1998. neering, UNB, and currently holds the rank of Professor in that department. He
[12] W. G. Stevens, “The current-voltage relationship in human skin,” Med. is also a Research Consultant to the Institute of Biomedical Engineering, UNB.
Electron. Biol. Eng., vol. 1, pp. 389–399, 1963. His research interests are primarily in the area of biological signal processing.
[13] M. Yuwaraj, A. Gluzmann, P. Madsen, and H. Kunov, “Adaptive
stimulus artifact cancellation in otoacoustic emission testing,” in Proc.
20th Canadian Medical and Biological Engineering Conf., 1994, pp.
106–107. Bernard Hudgins (M’97) received the Ph.D. degree
[14] R. Grieve, P. A. Parker, and B. Hudgins, “Adaptive stimulus artifact can- from the University of New Brunswick (UNB), Fred-
cellation in biological signals using neural networks,” presented at the ericton, NB, Canada, in 1991.
17th IEEE EMBES Conf., Montreal, P.Q., Canada, Sept. 1995. He is currently a Senior Research Associate with
[15] S. Haykin, Neural Networks: A Comprehensive Foundation. New the Institute of Biomedical Engineering at UNB
York: Macmillan College, 1994. His primary research interests are in the area of
myoelectric signal processing for the control of
artificial limbs.
Dr. Hudgins was the recipient of a Whitaker
Foundation Investigator Award and recently spent
two years on a NATO workgroup assessing alterna-
tive technologies for cockpit applications. He has been the Region 7 (Canada)
representative on the IEEE EMBS Advisory Committee for the past two years.

Kevin Englehart (S’90–M’99) received the B.Sc.


degree in electrical engineering and the M.Sc and
Ph.D. degrees from the University of New Brunswick
(UNB), in 1989, 1992, and 1998, respectively.
Richard Grieve received the B.Sc. and M.Sc. He is currently an Assistant Professor of Electrical
degrees, both in electrical engineering, in the field and Computer Engineering, and a Research Con-
of biomedical engineering, from the University of sultant to the Institute of Biomedical Engineering at
New Brunswick, Fredericton, NB, Canada, in 1994 UNB. His research interests include neuromuscular
and 1996, respectively. modeling and biological signal processing using
He is currently employed at Newbridge Networks adaptive systems, pattern recognition, and time-fre-
in Kanata Ont., Canada. His research interests quency analysis.
include neural networks and their application to Dr. Englehart is a Registered Professional Engineer, and a member of the
DSP, and the use of such techniques in biomedical IEEE Engineering in Medicine and Biology Society, the IEEE Computer So-
signal processing. ciety, and the Canadian Medical and Biological Engineering Society.

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