SPECTRAL ANALYSIS OF OLFACTORY BULBAR RESPONSES IN RAINBOW TROUT
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1 Jap. J. Physiol., 23, , 1973 SPECTRAL ANALYSIS OF OLFACTORY BULBAR RESPONSES IN RAINBOW TROUT Toshiaki J. HARA, M. FREESE, and K. R. SCOTT Fisheries Research Board of Canada, Freshwater Institute, Winnipeg, Manitoba R3T 2N6, Canada Summary The olfactory bulbar responses induced by chemical stimulation of the nares of rainbow trout were computer analyzed into frequency components. The spontaneous activity of the bulb was predominated by low-frequency components (2-6 Hz). Upon stimulation this immediately shifted to high-frequency components (7-11 Hz). The peak frequency pattern was characteristic of each single chemical tested regardless of the stimulus intensity. Multi-peak spectra were obtained on stimulation with compound stimuli such as food extract. The frequency component coding mechanism for olfactory receptive discriminatory function in the olfactory bulb is discussed. Electroencephalographic (EEG) techniques have been used previously for studying the mechanism of olfaction in fishes (see reviews by HARA, 1970, 1971). In these studies a single parameter, the amplitude (time-domain) of the response has been considered the coding mechanism for receptive discrimination of chemical stimuli. However, the amplitude of the response may be of limited importance, since it varies also with changing intensities of the same stimulus. The EEGs can be analyzed in terms of their frequency content. One of the most rigorous methods of analyzing such data is spectral analysis. It describes amplitude as a function of frequency (frequency-domain) rather than of time. An active band-pass filter was introduced to analyze the frequency components of the olfactory bulbar responses in fish (SATOU, 1971; UEDA et al., 1971; KUDO et al., 1972). However, the use of such filters suffers from technical limitations. The present studies deal with analysis using autocorrelation function of olfactory bulbar responses and their subsequent Fourier transforms. An attempt was made to establish a frequency-component coding mechanism in the olfactory bulb of fish. Received for publication April 17,
2 326 T. J. HARA, M. FREESE, and K. R. SCOTT MATERIALS AND METHODS Rainbow trout, Salmo gairdneri, about 20 cm in length, were used. Experimental procedures were essentially the same as those employed previously (HARA, 1973; HARA et al., 1973). Several amino acids, food extract and a hand rinse (a forefinger dipped in 100 ml water for 10 sec, were used as stimulants, all of which are effective olfactory stimulants for fish (HARA, 1973). EEG responses from the olfactory bulb were simultaneously recorded on a Grass model 7B polygraph and on a Precision Instrument model PI-6204 instrumentation tape recorder for later data analysis. Starting at 4 sec before the onset of the stimulus, 24-sec segments of the EEG response for each stimulant were chosen for spectral analysis. Each segment was further divided into twelve 2-sec segments (Fig. 1). For comparison, 4-sec and 10-sec segments (4- and 10-sec lag time) were also employed. Fig. 1. The 24-sec segments, starting at 4 sec before the onset of stimulus, of the bulbar response for each stimulant were subdivided into twelve 2-sec segments (arrows). The period of stimulation (10 sec) is shown by a heavy line below the EEG tracing. The autocorrelation function for each segment was calculated using a Hewlett-Packard model 3721A correlator. The correlator approximates the autocorrelation function of a given waveform X(t) by sampling the signal every ƒ t seconds, and then summing a finite number, N, of the sample products according to the equation, where z = qƒ z. is the lag time, and N is the number of samples. The range of z over which C(07) is of interest depends on the bandwidth of the signal X(t). A sampling interval of 10 msec was employed throughout the experiment. The resultant values were punched out on paper tapes, and these were then read into a computer (IBM 360). The power spectrum density (PSD) was calculated from the 100 correlation values, C(qƒ ƒñ), according to the equation (BLACK- MAN and TUKEY, 1958),
3 SPECTRAL ANALYSIS OF OLFACTORY RESPONSES 327 A refined estimate of the PSD was computed using a hanning window (BLACKMAN and TUKEY, 1958) to improve the frequency selectivity. A narrow bandwidth of the estimates was required to resolve the response peaks so that small shifts of these peaks might be observed. ; However, concomitant with an improvement in the resolution, the stability of the PSD estimates was unavoidably decreased. To obtain a sufficiently narrow bandwidth, yet maintain a measure of stability, the frequencies were computed at 1 Hz intervals. RESULTS The responses elicited in the olfactory bulb by chemical stimulation of the olfactory epithelium differed in amplitude for different locations of the recording electrodes. Normally, they were largest at the posterior and smallest at the anterior of the bulb. Typical responses recorded from anterior, middle, and posterior regions by application of 10-4 M L-serine are shown in Fig. 2. Fig. 2. Typical responses recorded from anteror, medial, and posterior regions of the olfactory bulb of the same fish when the nares were stimulated with 10-4 M L-serine. ON, olfactory nerve; OB, olfactory bulb; TC, telencephalon. A heavy line below the EEG tracing indicates the period of stimulus (10 sec). Figure 3 shows the three-dimensional (time, frequency, and power) presentation of the behavior of the bulbar responses to 10-4 M L-serine (A) and 10-5 g/ml food extract (commercial fish-food pellets) (B). Each curve for a 2-sec segment, starting at the first 2-sec, was plotted where not hidden by any of the curve previously plotted. Lower frequency components, ranging from about 2 to 6 Hz, were usually prominent in the spontaneous activity of the resting state before and after stimulation. On stimulation with L-serine, a peak appeared at approxi-
4 328 T. J. HARA, M. FREESE, and K. R. SCOTT Fig. 3. The three-dimensional description of time-frequency behavior of the olfactory bulbar responses to 10-4 M L-serine (A) and 10-5 g/ml food extract (B). Each curve is plotted where it is not hidden by any of the curves previously plotted. mately 12 Hz. This peak then shifted to a slightly lower range ( Hz; mean, 9.6 Hz) during the remainder of the stimulation period. In contrast, food extract produced various peaks with different power densities at different frequencies with various time lapses during stimulation. Four groups of peak frequencies could be identified at , , , and Hz. The food extract was a mixture of numerous chemical components, each of which could have a characteristic peak frequency range. Human hand rinse is an effective olfactory stimulant for some fish (HARA, 1973; HARA et al., 1973). L-Serine had been known to be one of the active components of the mammalian skin repellent to Pacific salmon (BRETT and MACKINNON, 1954; IDLER et al., 1956). The frequency analysis of a response to hand rinse (a forefinger dipped in 100 ml water for 10 sec) showed that the major frequency components ranged uniformly from 8.5 to 9.5 Hz (mean = 9.1 Hz), which was close to the range of the response to L-serine described above. Figure 4 shows the frequency spectra of the bulbar responses from posterior (A), medial (B), and anterior (C) regions of the bulb when the nares were stimulated with several concentrations of L-serine. A lag time of 10 sec was employed for this figure. Peak frequency ranges were consistent in all three regions regardless of the stimulus intensity. In the posterior region, for instance, the peak frequencies ranged from 8.5 to 9.2 Hz (mean = 8.9 Hz). Those of medial and anterior regions were Hz (mean = 9.0 Hz) and Hz (mean = 8.6 Hz), respectively. The extra peaks at lower frequencies ( Hz) in the anterior region (C) were due to background activity which was immediately interrupted by an oscillatory potential that was terminated by rinsing, if the
5 SPECTRAL ANALYSIS OF OLFACTORY RESPONSES 329 stimulus intensity was high. If, however, the stimulus intensity was low, only parts of the background activity were shifted, and the remainder was unchanged. Less power density in the spectrum density reflected less amplitude (time-domain) of the response. Fig. 4. The frequency-power spectra of the responses recorded at posterior (A), medial (B), and anterior (C) regions of the olfactory bulb when stimulated with 10-4 (closed circle), 10-5 (open circle), 10-6 (cross), and 10-7 (triangle) M L-serine. A lag time of 10 sec was employed. Figure 5 illustrates the frequency spectra of the bulbar responses recorded from the posterior (A), medial (B), and anterior (C) regions of the bulb, when stimulated with L-serine, D-serine, L-glutamine, hand rinse and food extract. A lag time of 10 sec was used here. In the posterior region, the peak frequency of each response to all stimulants but food extract fell into a narrow band, 9.1-
6 330 T. J. HARA, M. FREESE, and K. R. SCOTT Fig. 5. The frequency-power spectra of the responses recorded at posterior (A), medial (B), and anterior (C) regions of the olfactory bulb when stimulated with 10-4 M L-serin (closed circle), 10-4 M D-serine (open circle), 10-4 M L-glutamine (cross), hand rinse (triangle), and 10-5 g/ml food extract (square). A lag time of 10 sec was employed.
7 SPECTRAL ANALYSIS OF OLFACTORY RESPONSES Hz, whereas at least four peaks, at approximately 5.2, 8.8, 10.7, and 15.0 Hz, were observed on the spectrum of the response to food extract. These four peaks corresponded well with four peak groups found earlier in the spectra computed from 2-sec EEG segments (Fig. 3B). General features of the frequency spectra of the responses in the medial region were more or less similar to those of the posterior region except that the spectrum for hand rinse had an extra peak at approximately 5.0 Hz. Also, the peak seen at 15.0 Hz for food extract in the posterior region was not evident here. In the anterior region, responses were relatively small except for that to food extract, which, as mentioned above, was represented by higher spectral density of the background activity at lower frequencies. The results described above clearly indicate that each chemical stimulant has its own spectral pattern which can provide a basis for coding the quality of the stimulant within the olfactory bulb. DISCUSSION There has long been a controversy on the appropriateness of Fourier analysis for EEG which is more representative of a stochastic than a deterministic process. This is based on the fact that information about transients and phase relations is lost during the computations (see KLEMM, 1969). However, usefulness of the technique has recently been well described (Joy et al., 1971). The data here indicate that major activities of both background and induced response in the olfactory bulb of rainbow trout have relatively narrow frequency spectra. This is in sharp contrast to the mammalian EEG in which frequency extends to 125 Hz (HUGHES and HENDRIX, 1967; HUGHES et al., 1969). However, even lower frequency spectra have been reported in other salmonid fish species (KUDO et al., 1972); no difference was found in frequency ranges between spontaneous background activity and induced response in hime and chum salmon. There was no shift in frequencies such as those observed in the present analysis. It is uncertain whether such discrepancies are due to difference of species, since other factors such as recording and analysis techniques are also different. Similarity of the frequency spectra observed among the responses to L-serine, D-serine and L-glutamine (Fig. 5) can probably be explained by a common receptor site and nervous channel through which olfactory stimulation is initiated and conveyed. Effectiveness of amino acids as olfactory stimulants has been shown to depend largely on relative positions of their amino and carboxyl groups (HARA, 1973). The frequency spectrum of the response to food extract is of most significance. It clearly suggests that each active component or component group of the extract is likely to have its own peak frequency range detectable by the present technique. No attempt has been made so far to isolate active components from food extract. The identification of these active components, combined with chemical fractiona-
8 332 T. J. HARA, M. FREESE, and K. R. SCOTT tion, will provide further significant clues for understanding olfactory reception in aquatic animals in general. The frequency spectra shown in Figs. 4 and 5 well illustrate general features of frequency distribution during stimulation. However, time and phase relation, especially in the case of food extract, are obscure because of longer lag time. Variations in temporal patterns are well demonstrated in the dynamic presentations of Fig. 3. Evidently, the time lapses among the four peaks observed in the spectra of food extract differ in different regions of the olfactory bulb. Such spatiotemporal differentiations in the bulb may partly depend on different diffusion rates and mucous solubilities of stimulant chemicals. The time-space encoding of the frog mucosal response to odors has been suggested by MOZELL (1964). Chemical analysis of a repellent from human skin indicated that among substances identified only L-serine elicited a strong repellent action at extremely high dilution in Pacific salmon (IDLER et al., 1956, 1961). The single peak observed in the spectrum of the response elicited with hand rinse in the present experiments may largely represent the activity of L-serine existing in human hand rinse. The results of these preliminary examinations indicate that frequency spectral analysis of olfactory bulbar responses may provide possibilities for a more precise description of the underlying mechanism of chemoreception which plays an important role in such aspects of fish behavior as feeding, defense, and migration. The authors thank Dr. K. Ueda, Zoological Institute, University of Tokyo, for his advice, Miss Y.M.C. Law for technical assistance, and Miss C. Boyce for drafting. REFERENCES BLACKMAN, R. B. and TUKEY, J. W. (1958) The Measurement of Power Spectra, Dover, New York, p BRETT, J. R. and MACKINNON, D. (1954) Some aspects of olfactory perception in migrating adult coho and spring salmon. J. Fish. Res. Bd. Can., 11: HARA, T. J. (1970) An electrophysiological basis for olfactory discrimination in homing salmon: a review. J. Fish. Res. Bd. Can., 27: HARA, T. J. (1971) Chemoreception. In Fish Physiology, ed. by HOAR, W. S. and RANDALL, D. J. Adacemic Press, New York, Vol. 5, pp HARA, T. J. (1973) Olfactory responses to amino acids in rainbow trout, Salmo gairdneri. Comp. Biochem. Physiol., 44A: HARA, T. J., LAW, Y. M. C., and VAN DER VEEN, E. (1973) A stimulatory apparatus for studying the olfactory activity in fishes. J. Fish. Res. Bd. Can., 30: HUGHES, J. R. and HENDRIX, D. E. (1967) The frequency component hypothesis in relation to the coding mechanism in the olfactory bulb. In Olfaction and Taste, ed. by HAYASHI, T. Pergamon Press, Oxford, Vol. II, pp HUGHES, J. R., HENDRIX, D. E., WETZEL, N., and JONSTON, J. W., Jr. (1969) Correlation between electrophysiological activity from the human olfactory bulb and the subjective response to odoriferous stimuli. In Olfaction and Taste, ed. by PFAFFMANN, C. The Rockefeller University Press, New York, Vol. III, pp
9 SPECTRAL ANALYSIS OF OLFACTORY RESPONSES 333 IDLER, D. R., FAGERLUND, U. H. M., and MAYOH, H. (1956) Olfactory perception in migrating salmon. I. L-Serine, a salmon repellent in mammalian skin. J. Gen. Physiol., 39: IDLER, D. R., MCBRIDE, J. R., JONAS, R. E. E., and TOMLINSON, N. (1961) Olfactory perception in migrating salmon. II. Studies on a laboratory bioassay for homestream water and mammalian repellent. Can. J. Biochem. Physiol., 39: JOY, R. M., HANCE, A. J., and KILLAM, K. F., Jr. (1971) Spectral analysis of long EEG samples for comparative purpose. Neuropharmacology, 10: KLEMM, W. R. (1969) Animal Electroencephalography, Academic Press, New York, p KUDO, Y., SATOU, M., KAJI, S., and UEDA, K. (1972) Frequency analysis of olfactory response in fish by band-pass filters. J. Fac. Sci. Univ. Tokyo, Sec. IV, 12: MOZELL, M. M. (1964) Olfactory discrimination: electrophysiological spatiotemporal basis. Science, 143: SATOU, M. (1971) Electrophysiological study of the olfactory system in fish. I. Bulbar responses with special reference to adaptation in the carp, Cyprinus carpio L. J. Fac. Sci. Univ. Tokyo, Sec. IV, 12: UEDA, K., HARA, T. J., SATOU, M., and KAJI, S. (1971) Electrophysiological studies of olfactory discrimination of natural waters by hime salmon, a land-locked Pacific salmon, Oncorhynchus nerka. J. Fac. Sci. Univ. Tokyo, Sec. IV, 12:
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