Development of the auditory sensitivity and formation of the ...

ISSN 00220930, Journal of Evolutionary Biochemistry and Physiology, 2006, Vol. 42, No. 6, pp. 691—698. © Pleiades Publishing, Inc., 2006. Original Russian Text © E. V. Korneeva, L. I. Aleksandrov, T. B. Golubeva, and V. V. Raevskii, 2006, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2006, Vol. 42, No. 6, pp. 548—553.

COMPARATIVE AND ONTOGENIC PHYSIOLOGY

Development of the Auditory Sensitivity and Formation of the Acoustically Guided Defensive Behavior in Nestlings of the Pied Flycatcher Ficedula hypoleuca E. V. Korneevaa, L. I. Aleksandrov a, T. B. Golubevab, and V. V. Raevskii a a Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences,

Moscow, Russia b Department of Vertebrate Zoology, Lomonosov Moscow State University, Moscow, Russia

Received February 6, 2006

Abstract—Age dynamics of generation of the evoked potentials (EP) in the field L of caudal ni dopallium (the higher integrative center of the avian auditory system) and development of the audi toryguided defensive behavior were studied in control and visually deprived pied flycatcher Ficedu la hypoleuca nestlings. It was shown that the rhythmically organized monofrequency signals with sound frequency 3.5 kHz and higher produced the defensive behavior as the auditory sensitivity to these frequencies matured. After 9 days, the speciesspecific alarm signal produced more effectively the defensive behavior than the tonal signals. The rhythmically organized sound with filling fre quency 0.5 kHz, occupying the less lowfrequency diapason than the feeding signal, produced the effect opposite to the alarm signal to increase the nestling mobility. At the initial stage of the defen sive behavior development the auditory threshold fell markedly in the frequency diapason corre sponding to the frequency diapason of the alarm signal (5–6 kHz), which seemed to facilitate in volvement of this diapason signals in the defensive integration. The auditory EP generation thresh olds in the whole studied diapason were lower in the visually deprived nestlings than in the normally developing one; however, the ability of the acoustic signals to suppress alimentary reactions fell significantly. Key words: ontogenesis, defensive behavior, auditory sensitivity, field L, visual deprivation, birds, pied flycatcher. DOI: 10.1134/S0022093006060056

INTRODUCTION The nestlings of the hollownest pied flycatcher Ficedula hypoleuca are a convenient object to study formation of the earliest behavior forms. At once after the hatching they have auditory sensitivity in narrow diapason of low and intermediate frequen cies. The hearing is included in providing behav ior at the early stage of its structural and functional maturation, long before reaching the maturation level characteristic of adults [1]. The auditory sen

sitivity diapason is enlarged with age and thresh olds decrease. At the 5th day of life the diapason of frequencies perceived by nestlings reaches 8 kHz [2–4]. Study of the early ridiculous behavior of the pied flycatcher nestlings has allowed revealing a change of sensory stimuli producing their alimen tary behavior and connected with involvement of vision at the 5–6th day [3]. Only the complex of the acoustic signals including the parent’s feeding signal with the energy maximum in the area of 1– 4 kHz field produces the nestling feeding behavior

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from the hatching moment till 5–6 days. Since the 5–6th day the feeding behavior begins to appear at the illumination gradient that appears by the adult bird flying in the log house. From the 8–10th day, apart from the illumination gradient, the formed visual stimulus—the moving bird silhouette—also begins to participate in the behavior organization. At the last nest life stage (12–14 days) the feeding behavior is produced only by the formed visual stimulus. The defensive behavior in birds appears in the course of ontogenesis several days after the feed ing behavior. The defensive reaction at the moment of its appearance is associated with the speciesspe cific acoustic signalization (alarm signal) [4–8]. The energy maximum of the rhythmic alarm sig nal of the pied flycatcher is 5.0 kHz, while the up per limit is in the area of 6.0 kHz. It is used to think that the defensive behavior appears in nestlings in the middle of the nest period practically simulta neously with the eye opening [9–11]. Our previ ous works have shown that the first signs of the de fensive behavior in the form of cessation of feed ing reaction ending at acoustic signal sounds are recorded in the pied flycatcher nestlings 2–3 days prior to the eye opening [12, 13]. We have also es tablished that the normal acoustically guided de fensive behavior is not formed at visual depriva tion, particularly the hiding posture is absent [14]. However, any detailed analysis of dynamics of de velopment of the pied flycatcher auditory behav ior at the period of the defense behavior formation, in parallel with a study of a change of the role of the rhythmic signal proportion in the effectivity of stimulation of the defense behavior was not per formed. The goal of the present work was to trace dynamics of development of the auditory sensitiv ity in the normally developing and the visually de prived nestlings and to compare it with formation of the acoustically guided defensive behavior. MATERIALS AND METHODS The auditory evoked potentials (EP) from the field L of caudal nidopallium (the higher integra tive center of the avian auditory system) were re corded under laboratory conditions in the con scious pied flycatcher nestlings, free moving in the artificial thermostatic nest in response to presen

tation of sounds of clear tones of various frequen cy and intensity. The development of hearing was studied in 36 normally developing nestlings aged from 3 to 11 days and in 12 visually deprived nest lings at the age of 10 days. The sound source was an isodynamic head with the flat film diffuser fixed in the echoproof camera at the distance of 12 cm above the nestling head. The series of stimuli of various frequency and intensity (25 realizations in each) were presented in the quasirandom order. The acoustic stimuli were represented by the 20 ms long sounds of the clear tone, with the 2ms long fronts of an increase and decrease, of the filling fre quency 0.3–8 kHz. The interimpulse intervals, sta ble in each series, varied within the limits from 3 s (for older nestlings) to 30 s (for younger nestlings). The recording silver ball electrodes were im planted bipolarly in the field L of the nestlings un der the Nembutal anesthesia (0.1 mg/g of body mass, intraperitoneally). After amplification and filtration (the transmission band of 1–150 Hz), the signal was fed the computer to be averaged there in the real time by 25 realizations (the analysis ep och 250 ms, 1 ms in the channel). The beginning of the analysis epoch was synchronized with the beginning of the tonic signal presentation. The level of the sound pressure of the tone sound was determined using a Robotron USP measurer by the standard procedure: the USP of the “infin itive tone” was measured and the amplitude of the output signal of the USP measurer was fixed; then the amplitude of the tonal signals was chosen in such a way that the amplitude of the output signal of the measurer would be equal to the signal am plitude at infinitive tone sounding. The sound sig nals of the required amplitude were generated us ing the program. The tonal signal USP at the threshold evaluation was controlled by means of the USP measurer. Below the noise level the di rect control became impossible and the signal USP values were determined from data of a digital at tenuator. The generation thresholds of the auditory EP were determined from the averaged responses. Since the absolute threshold is not a fixed value, as responses to the nearthreshold stimuli are of the probability character, the threshold was considered the minimal sound pressure level, at which the av eraged response was detected, whereas no response

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was observed at the averaging of the same realiza tion number in the case of presentation of the sub threshold signal. In most cases, when using the sound threshold level (as determined from express ing of the averaged response), the probability of individual EP in the series of 25 presentations ap proached 50%. The study of establishment of the defensive be havior of the pied flycatcher nestlings was per formed under conditions of their natural feeding by the parents in 11 normally developing hatches (53 nestlings) and 8 hatches of the visually deprived nestlings (38 birds). At once after hatching the nest lings were placed in the experimental log house with the opening back wall, which was placed into s special camera, in which the researcher and the equipment were located. The visual deprivation was performed from the 1st day of the nestling life by sealing their eyes by the lightproof caps. The caps from the nestling eyes were removed at the age 12 days. All nestlings were examined and weighted daily, before the beginning of recording of behavior. Thus, both the normally developing and the visu ally deprived nestlings were submitted by the same manipulations. There were studied the effect on behavior of the taperecorded speciesspecific alarm signal (SSAS) whose energy maximum was 5 kHz and the effect of the rhythmically organized sounds of the clear tone of 0.5, 3.5, and 7 kHz. These frequencies are located outside the limits of the alarm signal spec trum and are mostly indifferent for producing the feeding or defensive behavior in nestlings of the studied age [4]. The rhythm and duration of the tonal sounds imitated the correspond parameters of the alarm signal (2 in 1 s, with the single sound duration of 125 ms); the sound pressure level was 70–75 dB, what also is equal to the sound pressure of the alarm signal recorded in the log house and produced by parents from outside. Each of the sig nals was presented as 2–5min long series, 3– 5 times per 24 h. The interseries interval amount ed to 15–30 min. The acoustic alimentary signals were presented to the nestlings independently and on the back ground of the abovementioned signals. The num ber of nestlings with the feeding reaction and du ration of the feeding reactions of individual nest

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Fig. 1. Age dynamic of change of the generation thresh olds of auditory evoked potentials from L field in nor mally developing nestlings. Abscissa: signal filling fre quency (kHz), ordinate: EP generation threshold (dB).Age (days): (1 ) 3, (2 ) 4, (3 ) 5, (4 ) 6, (5 ) 7, (6 ) 8, (7 ) 9, (8 ) 10, (9 ) 11.

lings were determined. The mean duration of the feeding reaction was calculated by summing up duration of feeding reactions of individual nestlings and dividing the total by the whole number of nest lings in the hatch. Efficiency of action of acoustic signals (i.e., their suppression of feeding reactions) was calculated by the following formula: 1 – t/T, where t—the mean duration of feeding reactions to isolated feeding signals. The results were treated statistically by using paired Student’s criterion. The differences were considered statistically significant at p < 0.05. RESULTS In the 3day old nestlings, EP were recorded only as a response to the clear tone in the diapason of 0.3–5.0 kHz (Fig. 1). The maximal sensitivity area occupied the diapason from 1.0 to 4.0 kHz, its thresholds amounted to 47 dB (± 2 dB). At higher and lower frequencies—5.0 and 0.5 kHz, the sen sitivity threshold was higher and amounted to 64 ± 8 and 63 ± 2 dB, respectively. At the 4th day the thresholds at frequencies 2–4 kHz decreased by about 9 dB, whereas the thresholds at frequencies

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Fig. 2. Generation thresholds of auditory evoked po tentials from L field in the 10day old normally devel oping and visually deprived nestlings. Abscissa: signal filling frequency (kHz), ordinate: EP generation thresh old (dB). (1 ) Normally developing nestlings, (2 ) visu ally deprived nestlings. Asterisk designates statistically significant differences of parameters ( p < 0.05).

Fig. 3. Efficiency of inhibition of alimentary reactions by different signals in the normally developing nestlings. Abscissa: nestling age (days), ordinate: efficiency (n). Signal filling frequency (kHz): (1 ) 0.5, (2 ) 3.5, (3 ) 7, (4 ) SSAS.

0.3–1 kHz changed but slightly. Responses to 5.0 kHz became steadier (the threshold amounted to 56 ± 4 dB), while in response to signal of the

frequency 6.0 kHz, EP was recorded in 43% nest lings, the thresholds being very variable (71 ± 7 dB). At the 5th day, the responses were recorded in the whole studied diapason of frequencies (0.3– 8.0 kHz); however, sensitivity at frequencies 7 and 8 kHz was very low—the frequencies exceeded 70 dB. The sensitivity peak was steadily shifted to the area of 2.0–4.0 kHz, the thresholds within this diapason amounting already to 33–34 dB. The most markedly decreased were the thresholds at 5 and 6 kHz; the threshold at 5 kHz at this time amounted to 40 ± 8 dB. A fall of the thresholds was observed at all frequencies; at the 6th day, at the frequency of 7 kHz the thresholds decreased to 63 ± 6 dB. At the 7th day, the maximal sensitivity area was enlarged including the frequency of 5 kHz. Later, further slight threshold decrease occurred, more pronounced in the highfrequency area. Comparison of the auditory EP in response to the monotonal sounds in the normally developing and the visually deprived 10day old nestlings showed (Fig. 2) that the auditory sensitivity thresh olds 0.3 and 0.5 kHz frequencies practically did not differ (at 0.3 kHz—38 and 39 dB, at 0.5 kHz— 40 and 30 dB, respectively). The generation thresh olds of the auditory EP in the 1.0–5.0 kHz diapa son in the visually deprived nestlings were, on av erage, by 5 ± 1 dB lower than in control and dif fered from them statistically significantly ( p < 0.05). At the 6 kHz frequency, difference between the thresholds amounted to 7 ± 2 dB; however, this difference did not reach the statistically signifi cance due to a high dispersion. At the higher fre quencies, 7.0 and 8.0 dB, the EP generation thresh olds in the control and in the visually deprived nest lings did not differ. Study of the effect of the rhythmically organized signals on realization of the defensive behavior in control nestlings showed that from the beginning of testing (the 3rd day) the nestling feeding behav ior was inhibited by the alarm signal and rhythmic monotone signal with the 3.5 kHz exposure fre quency, the efficiency of the tonal sounds being higher (at 4th day, statistically significant—p < 0.001) (Fig. 3). The alarm signal efficiency in creased between the 4th and 5th days of the nest ling life from 0.2 to 0.6 ( p < 0.05), than a slight decrease to 0.45 was observed until the 8th day. Beginning from the 9th day, the alarm signal effi

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ciency in the normally developing nestlings rose rapidly ( p < 0.001) to practically approach 1 by the age of 11 days. The rhythmically organized signals with 7.0 kHz frequency became effective for inhi bition of the feeding reactions only at the 6th day. Comparison of these curves with the curve of the alarm signal efficiency showed no statistically sig nificant difference between them until the 8th day. At the 9th day the alarm signal efficiency was sta tistically significantly higher as compared with ef fect both of the 3.5 kHz signal ( p < 0.05) and of the 7 kHz signal ( p < 0.001). Presentation of rhythmically organized signals of the lowfrequency diapason—0.5 Hz promoted an increase of the total motor activity of nestlings, the alimentary reactions being not suppressed at all (Fig. 3, 1 ). Changes of the alarm signal efficiency in the vi sually deprived nestlings were similar with those observed in hatches of the normally developing nestlings for the first 8 days (Fig. 4). Later, a de crease of the efficiency occurred to reach the 0.2 parameter by the 12th day ( p < 0.001). Next day after the cap removal from eyes this parameter increased to 0.5 ( p < 0.05) and subsequently did not practically change. Comparison of the normal ly developing and the visually deprived nestlings showed the statistically significant lower values of the alarm signal efficiency in the deprived nestlings beginning from the 9th day ( p < 0.001). Compar ison of the efficiency dynamics of the tonal sounds with the alarm signal efficiency in the visually de prived nestlings did not reveal the statistically sig nificant difference between the curves both before and after the eye opening. DISCUSSION The alarm signal is one of the most important signals for birds. Although the alarm signals have their specific characteristics in different species, they have most often the common pattern: in the absolute majority of cases they represent rhythmi cally organized sounds. It is known from the liter ature data that in the recently hatched duck nest lings the most essential factor for initiating the de fensive behavior is frequency of the repeated acous tic sounds [16, 17]; on the other and, it was shown that the main organizing factor of the defensive

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Fig. 4. Efficiency of inhibition of alimentary reactions by different signals in the visually deprived nestlings. Designations as those in Fig. 3. Arrow—moment of ces sation of visual deprivation.

behavior in the pied flycatcher nestlings was fre quency of the rhythmic sound presentation [4]. The authors noted that the signal repetition fre quency also plays some role in organization of the reactions, as the rarely following signals of the de fensive diapason are of low efficiency for mainte nance of defensive integration. Our data specify the earlier made conclusions. We have demonstrated the defensive behavior to be produced at the ini tial stage of its development not only by the alarm signal, but also by rhythmic sounds of the inter mediate and highfrequency diapasons, with fre quencies being outside the limits of the alarm sig nal spectrum (3.5 and 7 kHz), whereas the low frequency signal 0.5 kHz does not produce the de fensive behavior. Comparison of the obtained data to the sequence of development of the auditory sensitivity showed that informative for the defensive behavior were signals of the diapason, in which the sensitivity appeared after formation of the “alimentary dia pason” that included 1.5–2.5 kHz. The rhythmi cally repeated signals with 0.5 kHz frequency have the effect opposite to the hiding—the motor activ ity in nestlings increases. The motor activity in duck embryos at the 20th incubation day, including the beak clap considered a precursor of alimentary re

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actions, is known to increase in response to the low frequency tonal signals [19]. In the pied flycatcher nestlings at the age similar to the duck embryo age by the functional activity the lowfrequency tonal signal also increases motor activity and stimulates alimentary behavior. The literature data indicate that in the adult an imals and human thresholds of the behavior reac tions are equal or lower than the thresholds of the auditory sensitivity, detected on the basis of elec trophysiological analysis of activities of various lev els of the acoustic system [20–23]. However, stud ies of the feeding behavior in the pied flycatcher nestlings have shown that thresholds of the appear ance of alimentary reactions are by about 10 dB higher than the EP generation thresholds [4]. Our results demonstrate that realization of the audito ryguided defensive behavior in response to SSAS and 7 kHz tones takes place when the auditory sen sitivity thresholds are in the studied diapasons is somewhat lower than 65 dB. Taking into account that in our experiments the sound pressure level of the test signals was 75 dB, the thresholds of the appearance of the behavior reaction in our case also were by 10 dB higher than the EP generation thresholds. It is suggested that realization of the formed behavior needs massive modalspecific af ferentation that cannot be provided by activation of a negligible number of the lowthreshold ele ments, as this occurs in the case of the formed be havior. The fall of EP generation thresholds between the 4th and 5th days correlates in time with a statisti cally significant increase of the alarm signal effi ciency. It is important that before this moment, at the 3–4th day, the rhythmic tonal sounds 3.5 kHz (at this time, the thresholds at this frequency amount to 45–50 dB) suppress the alimentary re actions more effectively as compared with the alarm signal, in which diapason the sensitivity still is low. It is to be noted that the most expressed threshold decrease was observed at all studied fre quencies at the period from the 4th to the 7th day, this decrease occurring in the frequency diapason corresponding to the diapason of the alarm signal (5–6 kHz); in this area the threshold fall was more than 35 dB, whereas in other frequency diapasons it did not exceed 20 dB. Such threshold decrease seems to facilitate involvement of signals of this

diapason in the defensive integration. Since the external acoustic meatus of the nest lings are located in the direct vicinity of eyeballs, it was necessary to rule out the alternative explana tion: at the nestling eye sealing, a shift of skin and deformation of the acoustic meatus were possible. This could produce a deterioration of hearing in the visually deprived nestlings; in this case, it is this fact that could account for the low alarm signal efficiency in these nestlings. The obtained results indicate that the auditory EP generation thresholds are lower in the visually deprived nestlings than in control nest lings of same age. Earlier it was shown that involve ment of vision in behavior, first as a diffuse photo sensititvity (the 4–5th day), then as the object vi sion (the 8–9th day) is accompanied by a delay of development of the auditory structures and audito ry sensitivity [1, 24, 25]. It can be suggested that the higher auditory sensitivity in the visually deprived nestlings is a consequence of the absence of the de lays of the auditory sensitivity development due to impossibility of the alimentary behavior reorgani zation and of a change of its leading afferentation from the auditory to the visual one. Thus, a decrease of the auditory sensitivity thresholds in the alarm signal diapason is an im portant, but certainly not the only determining fac tor of formation of the defensive behavior. The dis turbances in the defensive behavior formation in the visually deprived nestlings seem to indicate the necessity of the intersensory interactions. It is known from the literature that changes within the limits of one sensory system can lead to changes in others. Thus, a modification of the visual experi ence in owl nestlings leads to a change of adjust ment of auditory neurons at the sound localization [26, 27]. At the song learning in the singing birds the visual experience change results in a modifica tion of the structure of the subsequently performed song [28] or in a change of its reproduction [29]. We believe the adequate visual afferentation to be necessary for successful realization of the acousti callyguided defensive behavior and learning of the alarm signal differentiation. ACKNOWLEDGMENTS This work is supported by the Russian Founda tion for Basic Research (project no. 040448920)

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