Lawrence S. Frishkopf

Responses to Acoustic Stimuli from Single Units in the Eighth Nerve of the Bullfrog

Single unit recordings from the eighth nerve of the bullfrog reveal two strikingly different kinds of auditory units. Both kinds of units exhibit sharply frequency dependent sensitivity (tuning curves). “Simple” units are maximally sensitive to tone bursts of frequency between 1000 and 1500 cps. Their frequency sensitivity and their capacity to “follow” pulse stimuli are well‐matched to the spectral composition and pitch period, respectively, of the bullfrogs croak. Simple units cannot be inhibited by acoustic stimuli. “Complex” units are inhibited by acoustic signals in the frequency range from 300 to 1000 cps. Some complex units are excited by acoustic stimuli, some are excited by both acoustic and vibratory stimuli, and some are excited by vibratory stimuli alone. Complex units that can be excited by sound are most sensitive to frequencies between 200 and 700 cps. Simple and complex units probably derive from separate sense organs (the basilar and amphibian papillae, respectively) within the otic caps...

Neural coding in the bullfrog's auditory system a teleological approach

Anatomical and physiological studies in the peripheral auditory system of the bullfrog have shown that there are two auditory receptor organs within the frogs inner ear which are sensitive over nearly disjoint frequency ranges. Stimuli whose frequencies lie between these ranges have mainly an inhibitory effect upon the response of the nerve fibers that innervate the low-frequency organ. It has been shown that the mating call, which is produced by the male bullfrog and functions to evoke calling in other males, often contains energy peaks in just the frequency ranges to which the peripheral receptor organs are optimally sensitive. The auditory nerve fibers from both organs respond most vigorously to signals whose fine temporal structure is like that of the mating call, that is, to pulsatile signals having a repetition rate of about 100 per second. Behavioral studies employing synthetic croaks indicate that for a stimulus to evoke calling it is necessary that sufficient energy be simultaneously present in the frequency ranges that excite the two auditory organs; evoked calling can be suppressed by signal components which inhibit the neural responses from fibers that respond to energy in the low-frequency range. When spectral conditions are met, calling is maximal for signals which have a temporal structure that produces the maximum neural response. It is concluded that the periphery of the bullfrogs auditory system is specialized to detect the major spectral and temporal features of the mating call and that the evoked-calling response depends upon the simultaneous excitation of the peripheral auditory organs. The possible biological significance of the latter mechanism is discussed. The relation of the other calls that the bullfrog makes to the response characteristics of his peripheral auditory system is also considered, as well as comparable relations in other species of frogs.

Auditory Nerve: Electrical Stimulation in Man

Auditory perceptions produced in a person deaf to acoustic stimulation were studied by electrically exciting the auditory nerve through permanently implanted electrodes. Pulsed current as small as 1 microampere peak-to-peak could be perceived. Pitch, as reported by the subject, varied with electrode selection, current amplitude, and pulse repetition rate from about 70 to at least 300 pulses per second. Loudness increased with amplitude and duration of pulse stimuli, and to a lesser extent with repetition rate. The total range in amplitude of the stimulus, from threshold to an uncomfortable loudness, was 15 to 20 decibels. Simultaneous stimulation in separate electrodes produced a number of complex effects.

Peripheral Origin of Auditory Responses Recorded from the Eighth Nerve of the Bullfrog

Single‐unit recordings have been obtained from the posterior branch of the bullfrogs eighth nerve at points peripheral to the ganglion. These units can be fitted into the three classes (viz., simple, complex, and non‐auditory) that were established by Frishkopf and Goldstein in a previous study [J. Acoust. Soc. Am. 35, 1219–1228 (1963)]. The sequence in which units of different classes were encountered on any one electrode pass supports the hypothesis that the complex units originate in the amphibian papilla and the simple units originate in the basilar papilla.

Model of Neural Inhibition in the Mammalian Cochlea

There have recently appeared in the literature several independent reports of experimental studies of the responses of primary auditory neurons in a number of different mammals to tonal stimulation. These studies show that a primary neuron that responds to sound at one frequency can be inhibited by a second tone at a slightly higher or lower frequency, and they suggest that this inhibitory interaction occurs within the cochlea. On the basis of this evidence, we have considered the characteristics of a variety of possible inhibitory‐connection schemes among elements lying within the cochlea. All of these schemes can lead to a sharpening of the frequency sensitivity of any single neuron. One, based on the principle of shunting generator currents away from the site of neural excitation, and consisting of linear operations except for shunting, yields a nonlinear generator function similar to one that Weiss used to fit the input‐output data of single primary units of the cat to click stimuli. Apart from its possible application in the cochlea, shunting inhibition leads to theoretically interesting operations in sensory‐information processing.

Auditory Responses in the Medulla of the Bullfrog: Comparison with Eighth‐Nerve Responses

Responses to acoustic stimuli of neural units in the medullae of DIAL‐anesthetized bullfrogs (Rana catesbeiana) have been recorded with metal microelectrodes. In a number of ways, these units appear to preserve the peripherally encoded information conveyed in the auditory portion of the eighth nerve. As in the periphery, two classes of units can be identified on the basis of frequency sensitivity, a low‐frequency group that can be inhibited and a high‐frequency group that cannot. The range of frequency sensitivity of these units for excitation and inhibition is the same as for the corresponding primary units. In other ways, however, the neurons of the medulla transform the eighth‐nerve input. Weak facilitation of the response of a high‐frequency unit by a low‐frequency stimulus has been found in several units. Many low‐frequency units exhibit very rapid adaptation at their frequencies of maximum sensitivity, responding only to the onset of a tonal stimulus. The maximum repetition rate at which such NO units can respond synchronously to pulses is much lower than for the corresponding peripheral units. The ON response has been found only among low‐frequency units. High‐frequency units respond, with adaptation, throughout a stimulus and show synchronous responses to pulses at rates as high as, or higher than, their peripheral counterparts.

Ultrastructure of the Basilar Papilla in the Bullfrog

The basilar papilla is one of two auditory organs found within the inner ear of most species of amphibians. It is thought to be homologous to the cochlea of higher vertebrates. We have used the techniques of light and electron microscopy to study this organ. The papilla is a short, cartilaginous, tubular extension of the saccule, terminated at the end by a thin, flat, contact membrane that separates the endolymphatic and perilymphatic spaces. Hair cells and supporting cells are arranged semicircumferentially in parallel rows along a portion of the tube. The tectorial membrane hangs from a cord that spans a diameter of the tube. From the surface of each hair cell there projects a bundle of sensory hairs, consisting of a number of stereocilia and a single kinocilium located at one side of the bundle. All hair cells are oriented in the same direction: the kinocilium is located at that side of the hair cell nearest to the contact membrane. About 350 myelinated nerve fibers innervate approximately 60 hair cells. Only one type of synapse has been found, an afferent connection between hair cells and nerve terminals. Notably absent are synapses of the sort commonly associated with efferent innervation.

Excitation and Inhibition of Primary Auditory Neurons in the Little Brown Bat

Single‐unit activity has been recorded from a total of 80 primary auditory neurons within the internal meatus of the bat Myotis l. lucifugus. The frequency to which an individual unit was most sensitive (“best frequency” of the unit) was always found in the interval 10 to 85 kcps; the best frequencies of about 23 of the units lay between 40 and 80 kcps. Sensitivity of a unit was sharply dependent upon frequency. The rise in threshold for frequencies above the best frequency of the unit was abrupt (about 300 dB/octave), while for frequencies below the best frequency it was somewhat more gradual (about 100 dB/octave). In over 80% of the units tested, evoked activity could be inhibited by frequencies just above the excitatory range of the unit. Some units were inhibited by frequencies below, as well as above, the excitatory range, though this effect was more difficult to observe. The latencies of excitation and inhibition were sufficiently alike to suggest that inhibition of this type cannot be under efferen...

Responses of Auditory Units in the Medulla of the Cricket Frog

Responses to acoustic stimuli were recorded with metal microelectrodes from single units in the medullae of DIAL‐anesthetized cricket frogs (Acris crepitans and A. gryllus). In every animal, two disjoint regions of frequency sensitivity were found. Units of one type were most sensitive between 250 and 1000 cps. Thresholds for these units at their frequencies of maximum sensitivity ranged from 44 to 81 dB SPL (sound‐pressure level). Within this population were units that were also sensitive to vibrational stimuli. Units of the other type were most sensitive between 3500 and 3800 cps. Thresholds for these units ranged from 73 to 99 dB SPL. The frequency sensitivities of the two types of units are well matched to the spectral distribution of energy in the cricket frogs mating call. Although units of both types were found close together in the medulla, we were unable to find any evidence of interaction between them. Within each population, a wide variety of adaptation rates was found, ranging from very slowl...

Best Inhibitory Frequencies of Complex Units in the Eighth Nerve of the Bullfrog

Complex units in the bullfrog have Best Excitatory Frequencies (BEF) below 900 Hz, and can be inhibited by tones in a broad frequency range. A units Best Inhibitory Frequency (BIF) is always greater than its best excitatory frequency. A scatter diagram of BIF vs BEF for 38 units indicates that mean BIF increases as BEF increases.