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2.2 Classical Conditioning
Classical conditioning is the most commonly used technique in the study of fi sh
hearing. Classical conditioning, also called Pavlovian or respondent conditioning, is
an associative learning paradigm in which a conditioned stimulus (CS, e.g. tone) is
paired with an unconditioned stimulus (US, e.g. taste of food) and an unconditioned
response (UR, e.g. salivation); after repeated pairings, the CS (tone) alone can
invoke the UR (salivation). This technique has been used in fi sh hearing studies to
determine audiograms (Buerkle 1967 ; Fay 1969 ; Popper et al. 1973 ), frequency
discrimination (Fay 1970 ; Chapman and Johnstone 1974 ), sound source discrimination (Buwalda et al. 1983 ; Lu et al. 1996 ), and for auditory scene analysis (Fay
1992 , 1998 ). This form of conditioning has become a powerful tool because it uses
an innate response to a biologically potent stimulus that does not require voluntary
movement. After Bull ( 1928 ) showed that eels ( Anguilla vulgaris ) could be conditioned to vibratory stimuli using electric shock, many other studies showed that this
type of conditioning was generalizable. All of these methods use a form of a refl exive response, such as a defense response (Kenyon et al. 1998 ) or a suppression of
ventilation or cardiac activity (Fay 1969 ; Buwalda et al. 1983 ; Lu et al. 1996 ). In the
case of ventilation suppression (measured as a suppression of mouth or opercular
movements), a tone–shock paradigm is used with the unconditioned response measured as a temporary reduction in the frequency of opercular ventilation movements; this response is robust and easy to measure in most fi sh, especially goldfi sh
(Otis et al. 1957 ; Fay 1972 , 1988 , 1998 ). During the conditioning period, the fi sh
begins to associate the tone with a shock and in subsequent trials starts to suppress
ventilatory movements in the anticipation of the shock when the tone is heard. After
conditioning, the fi sh will suppress its ventilatory movements upon hearing the tone
alone, even in the absence of a shock. The stimulus tone can be altered with respect
to frequency or intensity to determine the fi sh’s frequency selectivity or absolute
hearing threshold.
In almost all species tested, classical conditioning methods have yielded the lowest auditory thresholds compared to other methods that measure auditory thresholds
including auditory physiology. The lower auditory threshold measures produced by
behavioral methods are, in part, likely due to higher order processing and integration of auditory information required for whole animal behaviors. However, classical conditioning methods also have some potential limitations. Although training
time is relatively short compared to the operant and avoidance conditioning paradigms, initial classical conditioning can still take ~40–50 trials for some fi sh species
(Fay 2009 ). Furthermore, because the unconditioned stimulus is often an electrical
shock, this might preclude the use of particular species that are sensitive to stressors, like certain cichlid species (Tavolga 1974 ; Allen and Fernald 1985 ). Classical
conditioning also requires constant retraining during the testing phase. Finally, animals can only be conditioned a limited number of times, which then reduces the
number of stimulus parameters that can be investigated, and subsequent stimulus
parameter training requires additional subjects and/or longer test times.
A.A. Bhandiwad and J.A. Sisneros
2.2 Classical Conditioning
Classical conditioning is the most commonly used technique in the study of fi sh
hearing. Classical conditioning, also called Pavlovian or respondent conditioning, is
an associative learning paradigm in which a conditioned stimulus (CS, e.g. tone) is
paired with an unconditioned stimulus (US, e.g. taste of food) and an unconditioned
response (UR, e.g. salivation); after repeated pairings, the CS (tone) alone can
invoke the UR (salivation). This technique has been used in fi sh hearing studies to
determine audiograms (Buerkle 1967 ; Fay 1969 ; Popper et al. 1973 ), frequency
discrimination (Fay 1970 ; Chapman and Johnstone 1974 ), sound source discrimination (Buwalda et al. 1983 ; Lu et al. 1996 ), and for auditory scene analysis (Fay
1992 , 1998 ). This form of conditioning has become a powerful tool because it uses
an innate response to a biologically potent stimulus that does not require voluntary
movement. After Bull ( 1928 ) showed that eels ( Anguilla vulgaris ) could be conditioned to vibratory stimuli using electric shock, many other studies showed that this
type of conditioning was generalizable. All of these methods use a form of a refl exive response, such as a defense response (Kenyon et al. 1998 ) or a suppression of
ventilation or cardiac activity (Fay 1969 ; Buwalda et al. 1983 ; Lu et al. 1996 ). In the
case of ventilation suppression (measured as a suppression of mouth or opercular
movements), a tone–shock paradigm is used with the unconditioned response measured as a temporary reduction in the frequency of opercular ventilation movements; this response is robust and easy to measure in most fi sh, especially goldfi sh
(Otis et al. 1957 ; Fay 1972 , 1988 , 1998 ). During the conditioning period, the fi sh
begins to associate the tone with a shock and in subsequent trials starts to suppress
ventilatory movements in the anticipation of the shock when the tone is heard. After
conditioning, the fi sh will suppress its ventilatory movements upon hearing the tone
alone, even in the absence of a shock. The stimulus tone can be altered with respect
to frequency or intensity to determine the fi sh’s frequency selectivity or absolute
hearing threshold.
In almost all species tested, classical conditioning methods have yielded the lowest auditory thresholds compared to other methods that measure auditory thresholds
including auditory physiology. The lower auditory threshold measures produced by
behavioral methods are, in part, likely due to higher order processing and integration of auditory information required for whole animal behaviors. However, classical conditioning methods also have some potential limitations. Although training
time is relatively short compared to the operant and avoidance conditioning paradigms, initial classical conditioning can still take ~40–50 trials for some fi sh species
(Fay 2009 ). Furthermore, because the unconditioned stimulus is often an electrical
shock, this might preclude the use of particular species that are sensitive to stressors, like certain cichlid species (Tavolga 1974 ; Allen and Fernald 1985 ). Classical
conditioning also requires constant retraining during the testing phase. Finally, animals can only be conditioned a limited number of times, which then reduces the
number of stimulus parameters that can be investigated, and subsequent stimulus
parameter training requires additional subjects and/or longer test times.
A.A. Bhandiwad and J.A. Sisneros