thumb|Volley Theory of Hearing demonstrated by four neurons firing at a phase-locked frequency to the sound stimulus. The total response corresponds with the stimulus.|397x397pxVolley theory states that groups of neurons of the auditory system respond to a sound by firing action potentials slightly out of phase with one another so that when combined, a greater frequency of sound can be encoded and sent to the brain to be analyzed. The theory was proposed by Ernest Wever and Charles Bray in 1930 as a supplement to the frequency theory of hearing. It was later discovered that this only occurs in response to sounds ranging from about 500 Hz to 5000 Hz.
Description
The volley theory was explained in depth in Ernest Wever's 1949 book, Theory of Hearing. Groups of neurons in the cochlea individually fire at subharmonic frequencies of a sound being heard and collectively phase-lock to match the total frequencies of the sound. The reason for this is that neurons can only fire at a maximum of about 500 Hz but other theories of hearing did not explain for hearing sounds below about 5000 Hz.
thumb|Harmonic waveform of a fundamental frequency L/2
Harmonic spectrums
Sounds are often sums of multiple frequency tones. When these frequencies are whole number multiples of a fundamental frequency they create a harmonic. When groups of auditory neurons are presented with harmonics, each neuron fires at one frequency and when combined, the entire harmonic is encoded into the primary auditory cortex of the brain. This is the basis of volley theory.
Phase-locking
Phase-locking is known as matching amplitude times to a certain phase of another waveform. In the case of auditory neurons, this means firing an action potential at a certain phase of a stimulus sound being delivered. It has been seen that when being played a pure tone, auditory nerve fibers will fire at the same frequency as the tone. Volley theory suggests that groups of auditory neurons use phase-locking to represent subharmonic frequencies of one harmonic sound. This has been shown in guinea pig and cat models.
In 1980, Don Johnson experimentally revealed phase-locking in the auditory nerve fibers of the adult cat. In the presence of -40 to -100 decibel single tones lasting 15 or 30 seconds, recordings from the auditory nerve fibers showed firing fluctuations in synchrony with the stimulus. Johnson observed that during frequencies below 1000 Hz, two peaks are recorded for every cycle of the stimulus, which had varying phases according to stimulation frequency. This phenomenon was interpreted as the result of a second harmonic, phase-locking to the stimulus waveform. However, at frequencies between about 1000 Hz and 5000 Hz, phase-locking becomes progressively inaccurate and intervals tend to become more random.
Pitch perception
Pitch is an assigned, perceptual property where a listener orders sound frequencies from low to high. Pitch is hypothesized to be determined by receiving phase-locked input from neuronal axons and combining that information into harmonics. In simple sounds consisting of one frequency, the pitch is equivalent to the frequency. There are two models of pitch perception; a spectral and a temporal. Low frequency sounds evoke the strongest pitches, suggesting that pitch is based on the temporal components of the sound.
Historically, there have been many models of pitch perception. (Terhardt, 1974; Goldstein, 1973; Goldstein proposed that through phase-locking and temporal frequencies encoded in neuron firing rates, the brain has the itemization of frequencies that can then be used to estimate pitch.
Frequency theory
Ideas related to the frequency theory of hearing came about in the late 1800s as a result of the research of many individuals. In 1865, Heinrich Adolf Rinne challenged the place theory; he claimed that it’s not very efficient for complex sounds to be broken into simple sounds then be reconstructed in the brain. Later, Friedrich Voltolini added on by proposing that every auditory hair cell is stimulated by any sound. Correspondingly, William Rutherford provided evidence that this hypothesis was true, allowing greater accuracy of the cochlea. In 1886, Rutherford also proposed that the brain interpreted the vibrations of the hair cells and that the cochlea did no frequency or pitch analysis of the sound. Soon after, Max Friedrich Meyer, among other ideas, theorized that nerves would be excited at the same frequency of the stimulus. Today, electronic oscillators are often used to create sinusoidal or square waves of precise frequencies.
Electrophysiology
Attempts to electrically record from the auditory nerve began as early as 1896. Electrodes were placed into the auditory nerve of various animal models to give insight on the rate at which the neurons are firing. In a 1930 experiment involving the auditory nerve of a cat, Wever and Bray found that 100–5000 Hz sounds played to the cat produced similar frequency firing in the nerve. This supported the frequency theory and the volley theory. This implies that sound is encoded by neurons firing at all frequencies of a harmonic, therefore, the neurons must be locked in some way to result in the hearing of one sound.
Hearing loss and deafness
Congenital deafness or sensorineural hearing loss is an often used model for the study of the inner ear regarding pitch perception and theories of hearing in general. Frequency analysis of these individuals’ hearing has given insight on common deviations from normal tuning curves, excitation patterns, and frequency discrimination ranges. By applying pure or complex tones, information on pitch perception can be obtained. In 1983, it was shown that subjects with low frequency sensorineural hearing loss demonstrated abnormal psychophysical tuning curves. Changes in the spatial responses in these subjects showed similar pitch judgment abilities when compared to subjects with normal spatial responses. This was especially true regarding low frequency stimuli. These results suggest that the place theory of hearing does not explain pitch perception at low frequencies, but that the temporal (frequency) theory is more likely. This conclusion is due to the finding that when deprived of basilar membrane place information, these patients still demonstrated normal pitch perception. Computer models for pitch perception and loudness perception are often used during hearing studies on acoustically impaired subjects. The combination of this modeling and knowledge of natural hearing allows for better development of hearing aids.