Expert Systems with Applications 31 (2006) 199–205 www.elsevier.com/locate/eswa Classification of electro-oculogram signals using artificial neural network Ayşegül Güven a, Sadık Kara b,* b a Department of Electronics, Civil Aviation College, Erciyes University, 38039, Kayseri, Turkey Department of Electrical and Electronics Engineering, Erciyes University, 38039 Kayseri, Turkey Abstract This research is concentrated on the diagnosis of subnormal eye through the analysis of Electrooculography (EOG) signals with the help of Artificial Neural Network (ANN). Multilayer feed forward ANN trained with a Levenberg Marquart (LM) backpropagation algorithm was implemented. The designed classification structure has about 94.1% sensitivity, 93.3% specifity and positive prediction is calculated to be 94.1%. The end results are classified as normal and subnormal eye. Testing results were found to be compliant with the expected results that are derived from the physician’s direct diagnosis. The benefit of the system is to assist the physician to make the final decision without hesitation. With the future evolution of this system tested on a more populated subject groups, there is always potential for on-line implementation as an auxiliary diagnostic tool on the Electrophysiology machines. q 2005 Elsevier Ltd. All rights reserved. Keywords: EOG; ANN; Subnormal eye 1. Introduction The human eye is a spherical structure with a radius of about 12 mm. The inside is filled with a transparent substance corpus vitreum. The retina covers the inside surface and holds the optically sensitive nerve ends. Furthermore, the retina holds nerve fibers which leave the eye through the optical disc (Sprelckelsen Grumstup, Johnsen, & Hensen, 1994). The eye has a standing electrical potential or charge across it, like a weak battery, with the front of the globe positive and back negative. The resting or ‘standing potential’ is generated largely by the trasepithelial potential across retinal pigment epithelium (RPE). It varies from one to several milivolts, depending upon the state of ambient retinal illumination, because light leads to a polarization of the basal pigment epithelial membrane that translates into changes in the transepithelial potential. Retinal illumination causes an initial rapid fall in the standing potential over 60–75 s (the ‘fast oscillation’) followed by a slow rise over 7–14 min. (the ‘light response’ or ‘slow oscillation’). The clinical electro-oculogram (EOG) measures the amplitude of the standing potential and * Corresponding author. Tel.: C90 352 4374901 32228; fax: C90 352 4375784. E-mail addresses: aguven@erciyes.edu.tr (A.̧ Güven), kara@erciyes.edu.tr (S. Kara). 0957-4174/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.eswa.2005.09.017 light response (Heckenlively, & Arden, 1991; Marmor, & Zrenner, 1993). In the EOG, the standing potential is measured indirectly, using the fact that the spatial orientation of a polarized eye is detected by skin electrodes placed nasal and temporal to the eye. Much of the changes in standing potential, however, can be monitored via the EOG. (Marmor & Zrenner, 1993) The clinical value of the EOG for diagnoses as well as following the course of certain diseases has been studied in retinitis pigmentosa, diffuse RPE disease, Best’s macular dystrophy, Stargardt’s disease, dominant drusen and chloroquine toxicity (Heckenlively, & Arden, 1991; Tasman, 1992). In biomedicine, the assessment of vital functions of the body often requires noninvasive measurements, processing and analysis of physiological signals. Examples of physiological signals found in biomedicine include the electrical activity of the brain—the electroencephalogram (EEG), the electrical activity the heart—the electrocardiogram (ECG), the electrical activity the eye—i.e. electroretinogram (ERG) and electrooculogram (EOG)—respiratory signals, blood pressure, temperature and speech signals (Lisboa, Ifeachor, & Szczepaniak, 2000). Often, biomedical data are not well behaved. They vary from person to person, are affected by factors such as medication, environmental conditions, age, weight, mental and physical state. Consequently, clinical expertise is often required for a proper analysis and interpretation of medical data. This has led to the integration of signal processing with 200 A. Güven, S. Kara / Expert Systems with Applications 31 (2006) 199–205 Fig. 1. EOG response sample with the components labeled. In the dark phase, the lowest potential (dark trough-Dt) is reached in 8–12 min. A bright light is then turned on and recordings continue at 1-min intervals with the potential increasing in amplitude until the highest point (light peak-Lp) is reached in 7–10 min. intelligent techniques such as neural networks, expert systems and fuzzy logic to improve performance (Lisboa et al., 2000). Our primary research motivation was to advance the research of subnormal (macular degeneration) eye and develop a novel decision making system for identification of this subnormalities. We employed the Artificial Neural Network (ANN) for the purpose of distinguishing between subnormal and normal eye. We have implemented an ANN that will not only simplify the diagnosis but also enable the physician to make a quicker judgment about the existence of eye disease more confidence. An ANN can determine its conditions and adjust itself to provide different responses by using inputs and desired outputs. The most important thing about an ANN is that it works as an expert system which will eventually help the physicians with the decision making process about the existence of subnormalities. Applications of ANNs in the medical field are numerous. The numerous applications exhibit the suitability of ANNs in pattern classification including diagnosis of diseases (Übeyli, & Güler, 2003), for example, photoelectric plethysmography pulse waveform analysis (Allen, & Murray, 1993), diagnosis of myocardial infarction (Baxt, 1990; Baxt, 1995), electrocardiogram analysis (Edenbrandt, Heden, & Pahlm, 1993; Hilera, Martinez, & Mazo, 1995), analysis of doppler shift signals (Güler, & Übeyli, 2003), differentiation of assorted pathological data (Dybowski, & Gant, 1995; Miller, Blott, & Harries, 1992) and electroretinogram classification (Lipoth, Hafez, & Goubran, 1991); however, neural network analysis of EOG signals is a relatively new approach. This research is concentrated on the diagnosis of subnormalities through the analysis of EOG signals with the help of an ANN. Most of the research in this area concentrative on auxiliary systems that will assist the physician with the decision making part of the diagnosis. The aim is to help the ophthalmologist interprent the output of the examination systems more easily and diagnose the problem more accurately (Lisboa et al., 2000). 2. Material and methods EOG signal acquisition was conducted by a Tomey Primus 2.5 electrophysiology unit in the Ophthalmology Department of Erciyes University Hospital. Representative EOG signal wave is seen in Fig. 1. The system of the block diagram of the set up is seen in Fig. 2. The test group consisted of 72 people composed of 32 normal and 40 subnormal eye subjects. The patient group having eye disease had an age range of 30–78 years (Mean ageZ52) and involved 18 male and 22 female patients. There were 14 male and 18 female people. The group had a mean age of 34 years ranging from 26 to 55 years. Fig. 2. Block diagram of the set up. A. Güven, S. Kara / Expert Systems with Applications 31 (2006) 199–205 201 2.1. Measurement of the EOG The importance of the clinical measurement of the EOG lies in the fact that the amplitude of the responce changes when certain luminance conditions are varied. Thus, if a patient is placed in darkness the potential will decrease, while if a bright light is put on following dark adaptation the potential will increase (Fig. 1). The relative ratio of amplitudes in dark and light gives an index of the RPE response to ionic changes. This ratio of the light-peak/dark-trough (Lp/DtZArden ratio) normally is 1.8 or greater. A ratio of 1.5 or less indicates a clearly abnormal RPE response. Generally a ratio of about 1.6 is considered the demarcation between normal and abnormal (Tasman, 1992). To standardize the test and maximize the response a specific protocol is used. Following a preadaptation period of several minutes to acquaint the patient with the test, the lights are turned off for 15 min. Recordings for several saccades are made in the dark at 1 min intervals. The lowest potential (dark trough-Dt) is reached is 8–12 min. A bright light is then turned on and recordings continue at 1-min intervals with the potential increasing in amplitude until the highest point (light peak-Lp) is reached in 7–10 min (Fig. 1) (Heckenlively, & Arden, 1991; Marmor, & Zrenner, 1993; Tasman, 1992). This electrical response is generated by the retinal pigment epithelium with the light peak being generate this potential it is likewise necessary to have intact photoreceptors which are apposed to the RPE (Tasman, 1992). Fig. 3. (a) Comparison of Dt values for the normal (32 person) and subnormal (40 person), (b) Comparison of Lp values for the normal (32 person) and subnormal (40 person). 2.2. Preparation of testing and training files The data which is recorded from all patients was used as input of the ANN. After the detection of the Dt and Lp values, feature extraction process is started. It can be seen in Fig. 3 where a comparison of amplitudes of the Dt and Lp EOG signals input values of ANN for the normal (32 person) and subnormal (40 person) eye. It is seen that, majority magnitudes of the Dt and Lp EOG signals similar to each other (normal and subnormal). These values were used as an input data for multilayer perceptron (MLP). During supervised learning, the ANN was trained on input vectors and the target output vectors with which it is required to associate the input vectors. The outputs are represented by unit basis vectors: [0 1] normal (Edenbrandt et al., 1993) subnormal Output vectors were determined from realized clinic findings these pattern electroretinography (PERG), angiography and Arden ratio of EOG. Fig. 4. The algorithm of the classification system. 202 A. Güven, S. Kara / Expert Systems with Applications 31 (2006) 199–205 Table 1 An example of a training set consists of random selected subjects Ann inputs Normal eyes Subnormal eyes Subject no 1 2 Subject no 1 3 8 11 15 18 23 28 37 40 184.33 526.12 208.74 672.61 139.16 511.47 292.97 625.00 421.14 917.97 391.85 481.97 253.71 312.06 506.85 684.24 429.72 550.04 363.86 520.31 2.3. The procedure of the classification system Fig. 4 shows the procedure used in the development of the classification system. It consists of four parts: (a) measurement of EOG signals, (b) neural network inputs were selected, (c) classification using neural network, (d) classification results. 2.4. Artificial neural networks An ANN is a mathematical model consisting of a number of highly interconnected processing elements organized into layers, the geometry and functionality of which have been likened to that of the human brain. An ANN is trained with the available data samples to explore the relation between inputs and outputs, so that you can reach the proper and accurate outputs when you input some new data (Simpson, 1989). A Multilayer feed forward ANN was implemented in the MATLAB software package (MATLAB version 5.3 with neural network toolbox). This choice is appropriate for solving pattern classification problems where supervised learning is implemented with a LM backpropagation algorithm. (An example of training set is seen in Table 1) A LM back propagation neural network was used for the interpretation of eye EOG waveforms. The advantage of using this type of ANN is the rapid execution of the trained network, which is particularly advantageous in signal processing applications. ANN training is usually formulated as a nonlinear least-squares problem. 2.4.1. Levenberg marquard backpropagation algorithm The backpropagation algorithm is a widely used training procedure that adjusts the connection weights of a MLP (Rumelhart, Hilton, & Williams, 1986). Essentially, the LM algorithm is a least-squares estimation algorithm based on the maximum neighborhood idea. As shown in Fig. 5, an MLP consists of three layers: an input layer, an output layer, and one or more hidden layers. Each layer is composed of a predefined number of neurons. The neurons in the input layer only act as buffers for distributing the input signals xi to neurons in the hidden layer. Each neuron j in the hidden layer sums up its input signals xi after weighting them with the strengths of the respective connections wij from the input layer, and computes its output yj as a function f of the sum: sigmoidal, hyperbolic tangent, or radial basis function. The output of neurons in the output layer is similarly computed (Beale, & Jackson, 1990; Güler, & Übeyli, 2003; Haykin, 1994; Türkoğlu, Arslan, & İlkay, 2002; Wright, & Gough, 1999). Training a network consists of adjusting the network weights using the different learning algorithms. A learning algorithm gives the change Dwij(t) in the weight of a connection between neurons i and j at time t. For the Levenberg-Marquardt learning algorithm, the weights are updated according to the following formula wij ðt C 1Þ Z wij ðtÞ C Dwij ðtÞ with Dwij Z ½JT ðwÞJðwÞ C mIK1 JT ðwÞEðwÞ where J is the Jacobian matrix, m is a constant, I is a identity matrix, and E(w) is an error function (Allen, & Murray, 1993; Baxt, 1990; Lisboa et al., 2000; Übeyli, & Güler, 2003). 2.5. Classification using neural network ANN underwent supervised learning to perform successful pattern recognition of the EOG signals. With sufficient training, the ANN should be able to classify correctly previously unseen input vectors. The network is iterated for single and double hidden layers with combinations of 1–10 neurons in each layer (Fig. 5). For each layer combination, the target mean square error was set to 0.1!10K4 and the epoch yj Z f ðSwij xi Þ where f is the activation function that is necessary to transform the weighted sum of all signals impinging onto a neuron. The activation function f can be a simple threshold function, a Fig. 5. Structure of ANN. A. Güven, S. Kara / Expert Systems with Applications 31 (2006) 199–205 203 Table 2 Test results Group type Real number of subjects in the test group True False Negative (normal) Positive (subnormal) Total SensitivityZ(TP)/(TPCFN) %Z%94.1 SpecifityZTN/(TNCFP) %Z%93.3 Positive predictivityZTP/(TPCFP) %Z%94.1 TP: true positive TN: true negative FP: false positive FN: false negative 15 17 32 14(%93.3) 16(%94.1) 30(%93.75) 1(%6.7) 1(%5.9) 2(%6.25) number was taken as 500. The train input data set consisted of 17 normal and 23 subnormal eye patients, while the test data set was made of 15 normal and 17 subnormal eye patients. The minimum training and testing errors were accomplished with the combination of single hidden layer consisting of five neurons. Hidden layer sigmoidal function and output layer linear function was used. The performance of the ANN algorithms was assessed by the following measures; (1) True Positive (TP): the ANN identifies an input as a subnormal eye that was labeled as a patient by the test. (2) True Negative (TN): the ANN identifies an input as a normal that was labeled as a healthy by the test. (3) False Positive (FP): the detection of a subnormal in an EOG and clinical findings that was labeled as a normal by the test. (4) False Negative (FN): the detection of normal in an EOG and clinical findings that was labeled as a patient by the test. The performance of the classifier is also assessed in terms of sensitivity and specificity as follows; (1) Sensitivity: a measure of the ability of the classifier to detect subnormal eye. Subjects having eye diseases are classified correctly with 94.1% and incorrectly with 5.9%. In this case, by using this network classification, normal subjects and patient subjects are classified with 93.3 and 94.1% accuracy, respectively. The sizes of mean square error (MSE) and mean absolute error (MAE) can be used to determine how well the network output fits desired output, a testing MSE of 0.0310 and MAE of 0.0508 was observed for our optimized MLP feed forward network with a training MSE of 5.5665!10K5 and MAE of 0.0048. The variation of system error rate with respect to the epoch number during training iterations is shown in Fig. 6. As seen in this figure, the results are stable and no fluctuations are observed. This indicates that the selected parameters are most proper set for a minimum rate. As seen in Table 2, 93–94% success rate of classification was accomplished with the designed feature extraction and the neural network structures. Final results were classified as normal and subnormal. There was one false classification in the negative group, while 14 subjects were correctly recognized as healthy. In the positive (subnormal eye) group, only one subject was misclassified, and 16 people were accurately classified as diseased. The overall results, shows that 93.75% correct classification was achieved, whereas two false classifications have been observed for the group of 32 people in total. With these results (the values of statistical parameters), this network has about 94.1% Sensitivity Z ðTPÞ=ðTP C FNÞ% (2) Specificity: a measure of the ability of the classifier to specify normal eye. Sensitivity Z ðTNÞ=ðTN C FPÞ% (3) Positive predictivityZ ðTPÞ=ðTPC FPÞ% 3. Results After the training phase, testing of the LM backpropagation neural network was established. The data, which has not been used as an input to the network, was applied to the network for testing the network performance. After the process, normal (healthy) subjects are classified correctly with 93.3% and incorrectly with 6.7% (Table 2). Fig. 6. Variation of the error rate with respect to the epoch number in the ANN. 204 A. Güven, S. Kara / Expert Systems with Applications 31 (2006) 199–205 Fig. 7. (a) Desired output result (normal), actual network output result (normal), (b) Desired output result (subnormal), actual network output result (subnormal). sensitivity, 93.3% specifity and positive prediction is calculated to be 94.1% (Table 2). The ANN test results belong to normal and subnormal patients were compared realized clinic findings (Pattern electroretinography (PERG), angiography and Arden ratio of EOG) belong to same persons. The outputs of actual network and desired network are set to vary within the range of 0–1. In Fig. 7(a), the output values of 15 subjects shows that all the normal subject values are one. The actual network output pattern characterized around 1 except one, which has the value 0. This means that one of 15 subjects was misclassified in the network. On the other hand, Fig. 7(b) illustrates the desired output values of 17 subjects are 1 and the actual network outputs are around 1 while one subject has the output value of 0. From this perspective, it explains that one of 17 subjects was misclassified in the network. 4. Discussion and conclusion The fuzzy appearance of the EOG signals sometimes makes physicians suspicious about the existence of eye diseases and causes false diagnosis. Our technique gets around this problem using ANN to decide and assist the physician to make the final judgment in confidence. The three layer MLP structure that we have built gave very promising results in classifying the normal and subnormal eyes. We are not claiming to replace the currently used devices for EOG. On the other hand, we are proposing a complimentary system that can be coupled to software of the ophthalmic electrophysiology devices. The benefit of the system is to assist the physician to make the final decision without hesitation. But, the limitation of this system that the system has had 6.25% misclassified result in the test since we selected some of data used from early phase of the macular degeneration. In this study, we believe that this research developed an expert system for the interpretation of the EOG signals using ANN. The stated results show that the proposed method can make an effective interpretation. Acknowledgements This project was supported as Post-Graduate Education and Research Project by Erciyes University (Project no. FBT04-27). References Allen, J., & Murray, A. (1993). Development of a neural network screening aid for diagnosing lower limb peripheral vascular disease from photoelectric plethysmography pulse waveforms, physiology. Measurement, 14, 13–22. Baxt, W. G. (1990). Use of an artificial neural network for data analysis in clinical decision making: The diagnosis of acute coronary occlusion. Neural Computing, 2, 480–489. Baxt, W. G. (1995). 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Ultrasound in Medicine and Biology, 24(5), 735–743. 205 Ayşegül Güven graduated from Electronics Engineering Department of Erciyes University with a BS degree in 1999 and is currently employed as an instructor at the department of electronics in the Civil Aviation School. Consequently, she is pursuing her PhD degree in Department of Electronics Engineering at Erciyes University and conducting her research in the area of biosignal processing and neural network applications in medicine. Sadık Kara graduated from the Faculty of Electronics Engineering, Erciyes University in 1988. He received his MS degree in 1991 and doctorate in 1995 from the Institute of Science, Erciyes University. He is presently working as an Associate Professor in the Bioelectronics branch of Electronics Engineering at the same institution. His general research interests include bioinstrumentation, biosignal processing and neural network applications in medicine. ID 389065 Title Classificationofelectro-oculogramsignalsusingartificialneuralnetwork http://fulltext.study/journal/431 http://FullText.Study Pages 7