Neuroscience and Behavioral Physiology, Vol. 40, No. 5, 2010
Effects of Visual Deprivation on the Development of Auditory Sensitivity during Formation of the Freezing Reaction in Pied Flycatcher Nestlings E. V. Korneeva,1 L. I. Aleksandrov,1 T. B. Golubeva,2 and V. V. Raevskii1
UDC 612.82
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 59, No. 2, pp. 180–184. March–April, 2009. Original article submitted April 10, 2008. Accepted June 9, 2008. Recording of evoked potentials from the higher center of the auditory system – field L of the nidopallidum – was used to study the formation of auditory sensitivity in normally developing and visually deprived pied flycatcher nestlings aged 6–9 days. Restriction of visual afferentation was found to produce significant reductions in the absolute threshold of auditory evoked potentials in the frequency range of the species-specific food call (1–3 kHz) during the period at which vision acquires a role in providing sensory support for feeding behavior in control nestlings (six days). In the frequency range of the species-specific alarm call (4–5 kHz), the thresholds of auditory evoked potentials were significantly lower than those in controls during the period at which vision acquires a role in providing sensory support for defensive behavior (8–9 days). Taking account of previous data showing decreases in the efficiency of acoustic signals in evoking freezing reactions in visually deprived nestlings, it is suggested that defensive behavior develops not simply as a response to the acoustic alarm call or tones imitating it, but as a system whose complete formation and functioning require integration of a series of factors, including visual afferentation. KEY WORDS: ontogenesis, behavior, vision, hearing, evoked potentials, birds, freezing.
Hearing and vision are the sensory systems whose maturation occurs latest during ontogenesis. The formation of auditory sensitivity begins before birth, initially at low frequencies, with subsequent widening of the range; the range at which sensitivity is maximal spreads to ever higher frequencies. The development of hearing in this direction is determined by the development of the cochlea of the inner ear and the sequential formation of the auditory epithelium during ontogenesis in birds [7, 8]. In precocial bird species, auditory sensitivity over virtually whole range appears during the embryonic period of development. At the moment of hatching, the altricial pied flycatcher can only hear in the range of low and intermediate frequencies, sen-
sitivity to the higher-frequency range 4–6 kHz appearing after four days. At hatching, vision does not function in pied flycatcher nestlings. Recording of evoked potentials from the Wulst showed that responses to flashes of light appeared on day 3 [6], though the retina lacked photoreceptors until day 5–6 [2]. During the first days after hatching, the only form of behavior in pied flycatcher nestlings – feeding – is triggered by acoustic signals. The species-specific parental feeding call is a wideband sound with a spectral maximum at 1.8–2.5 kHz, though nestlings demonstrate feeding reactions on presentation of short signal of any frequency within the range of their auditory sensitivity. From six days, feeding behavior starts to receive support from vision [6]. Defensive behavior in the form of the freezing reaction is the next identifiable type of behavior in nestlings – this can be evoked from age five days in natural conditions by rhythmically repeated acoustic alarm calls. Alarm calls occupy
1 Institute
of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow. 2 Department of Zoology, M. V. Lomonosov Moscow State University; e-mail:
[email protected].
479 0097-0549/10/4005-0479 ©2010 Springer Science+Business Media, Inc.
480 the frequency range 3.5–6.5 kHz, while the energy peak is at 4.5–5.5 kHz [3]. The inclusion of object vision into the sensory support of defensive behavior at 9–10 days coincides with the time at which the alarm call shows an increase in its ability to induce freezing [4]. Our previous studies demonstrated that restriction of visual afferentation in pied flycatcher nestlings prevents the normal formation of acoustically controlled defensive behavior. The effectiveness of the alarm call during the nesting period decreased in these nestlings. Even after the end of visual deprivation on day 12, alarm call effectiveness remained significantly lower than in control nestlings of the same age. Furthermore, visually deprived nestlings were unable to discriminate the species-specific alarm call from rhythmically organized bursts of a pure tone [4]. Restriction of afferentation during the critical period of development can impair the later ability to learn [5]. The aim of the present work was to address the dynamics of the formation of auditory sensitivity in control and visually deprived nestlings during the period at which vision is recruited into the sensory support for defensive behavior (6–9 days) to identify the characteristics of the formation of hearing in conditions of restriction of visual afferentation, hindering the recruitment of the alarm call into the execution of defensive behavior.
METHODS Auditory evoked potentials (EP) were recorded from field L of the nidopallidum (the higher integrative center of the auditory system in birds) [12] in laboratory conditions in conscious, freely moving (in an artificial temperaturecontrolled nest) pied flycatcher nestlings in response to bursts of pure tone in the range 0.3–8 kHz at different intensities. The development of hearing was studied in 29 normally developing and 28 visually deprived nestlings aged 6–9 days. The sound source was an isodynamic head with a flat film diffuser attached to a sound-absorbing chamber at a distance of 12 cm above the nestling’s head. Series of stimuli of different frequencies and intensities (25 trials per series) were presented in random order. Acoustic stimuli consisted of bursts of a pure tone of duration 20 msec with rise and decay times of 2 msec and filling frequencies of 0.3–8.0 kHz. The interstimulus interval was 3 sec. Silver ball recording electrodes were implanted in a bipolar regime into field L of nestlings under Nembutal anesthesia (0.1 mg/g, i.p.). After amplification and filtration (bandpass 1–150 Hz), signals were inputted into a computer for real-time averaging of sets of 25 trials (the analysis epoch was 250 msec, 1 msec per channel). The beginnings of analysis epochs were synchronized with the onsets of presentation of tonal bursts. The sound pressure of tonal bursts was assessed using a Robotron (DDR) sound pressure level (SPL) meter. Direct
Korneeva, Aleksandrov, Golubeva, and Raevskii measurement was impossible below the noise level and signal SPL values were measured using a digital attenuator. The absolute thresholds for auditory EP generation were determined using averaged responses. As absolute thresholds do not have any particular fixed values, because responses to near-threshold stimuli are essentially probabilistic in nature, the minimum sound pressure level at which the averaged response was distinguishable was taken as the threshold, no response being detected on averaging of the same number of trials with presentation of subthreshold signals. In most cases using the threshold sound level (defined in terms of the size of the averaged response), the probability of individual EP in series of 25 presentations was close to 50%. Statistical analysis was performed using the t test. Differences were regarded as significant at p < 0.05. Visual deprivation was performed in nestlings from day 1 of life by gluing opaque patches over their eyes. Patches were glued twice daily during the first three days and then once daily.
RESULTS In control nestlings, EP were recorded over the whole range studied at age six days, though responses to tonal bursts in the high-frequency and low-frequency areas were characterized by high thresholds. The lowest thresholds, specifying the region of the maximal sensitivity, were seen in response to tonal bursts in the range 2–4 kHz, where values were 25–30 dB. In visually deprived nestlings of the same age, EP generation thresholds at most of the frequencies studied were lower than the corresponding response thresholds in control nestlings. Thresholds in the region of maximal sensitivity were no greater than 18–25 dB. The differences between the EP thresholds of control and visually deprived nestlings at frequencies of 0.3, 1, 2, 3, and 8 kHz were significant (Fig. 1, A). It should be noted that the decrease in thresholds in visually deprived nestlings occurred mostly in the range of single-frequency signals evoking feeding responses in nestlings. On day 7, the region of maximum sensitivity widened to 5 kHz. EP thresholds in this region in control nestlings were 22–27 dB, compared with 14–20 dB in visually deprived nestlings. Comparison of frequency-threshold curves in control and visually deprived nestlings revealed a significant difference between values only at frequencies of 3 and 8 kHz (Fig. 1, B). On day 8, there were further reductions in EP thresholds at all frequencies. Response thresholds at the region of maximal sensitivity were 18–20 dB in control nestlings and 12–15 dB in visually deprived nestlings. Comparison of thresholds in control and visually deprived nestlings revealed significantly lower thresholds in visually deprived nestlings at all frequencies in the region 2–5 kHz (Fig. 1, C), i.e., visual deprivation produced significant reductions in
Effects of Visual Deprivation on the Development of Auditory Sensitivity
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Fig. 1. Threshold characteristics of auditory evoked potentials in controls (squares, continuous lines) and visually deprived (circles, dotted lines) nestlings. A) 6 days; B) 7 days; C) 8 days; D) 9 days. The abscissas show signal filling frequency, kHz; the ordinates show absolute EP generation thresholds, dB SPL. Thick horizontal lines above show the range covered by the spectrum of the species-specific alarm call and single-frequency signals evoking freezing reactions in nestlings. Thin lines show the range of single-frequency signals evoking feeding reactions. *p < 0.05.
thresholds, mostly in the region of the single-frequency signals evoking freezing reactions in nestlings. On day 9, thresholds in the region of maximal sensitivity were 16–17 dB in control nestlings and 10–13 dB in visually deprived nestlings. Thresholds in deprived nestlings were significantly lower over a wide range, from 1 to 5 kHz (Fig. 1, D).
DISCUSSION Adaptive changes occurring in pathological conditions can, as in normal conditions, be regarded as a systems process affecting the whole body and directed to achieving favorable outcomes [1]. Thus, loss of visual afferentation at an early age leads to compensatory rearrangements in the somatosensory and auditory analyzers [9–11]. Young animals adapt to changes in the spatial relationships between visual and auditory signals; the properties of their auditory neurons
change accordingly [13]. The results obtained here showed that restriction of visual afferentation leads to faster development of auditory sensitivity. In visually deprived nestlings, thresholds for auditory EP at frequencies of 1–3 kHz – the region containing the signals most effective for inducing feeding behavior – were significantly lower than those in control nestlings by day 6. By day 9, the range of significantly lower thresholds widened to 5 kHz, covering the region of the energy maximum of the species-specific alarm call. It is important to note here that in normal conditions, vision starts to provide sensory support for the nestlings’ feeding behavior from 5–6 days; on the other hand, visual afferentation starts to influence freezing from 9 days. In other words, restriction of visual afferentation decreases the thresholds of auditory EP in the frequency ranges important for feeding and defensive behaviors at the corresponding periods at which vision is recruited into providing sensory support for these types of behavior. However, our studies showed that restriction of visual afferentation in pied fly-
482 catcher nestlings prevents the normal formation of acoustically directed defensive behavior. The effectiveness of the alarm call during the nesting period decreased in these nestlings. Furthermore, visually deprived nestlings were unable to discriminate the species-specific alarm call from rhythmically organized bursts of pure tone [4]. The present experiments showed that in deprived nestlings of all ages studied, the absolute auditory sensitivity thresholds were not greater than those in control nestlings. As a result, impairments to the establishment and organization of passive defensive behavior in deprived nestlings cannot be associated with the fact that their auditory system provides insufficient support for the perception of the acoustic defensive signal. Thus, the compensatory reduction in the auditory sensitivity threshold is insufficient for performance of the full acoustically directed defensive behavior. This suggests that defensive behavior develops not simply as a response to the acoustic alarm call or tones imitating it, but as a system whose complete formation and functioning requires integration of several factors. Among several such factors, visual afferentation appears to have an important position, even though it does not have a direct role in organizing defensive behavior at the early stages of its development.
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1. Restriction of visual afferentation significantly decreases auditory EP thresholds in the frequency range of the species-specific feeding call during the period corresponding to the time at which vision is recruited into the sensory support for feeding behavior and in the frequency range of the species-specific alarm call during the period corresponding to the time at which vision is recruited into providing sensory support for defensive behavior. 2. Defensive behavior develops not simply as a response to an acoustic alarm call or tones imitating it, but as an integral system whose complete formation and functioning requires integration of a series of factors, including visual afferentation. This study was supported by the Russian Foundation for Basic Research (Project No. 07-04-01022).
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