Two-tone Inhibition Research Articles

Response properties underlying selectivity for the rate of frequency modulated sweeps in the auditory cortex of the mouse

This study focused on the response properties underlying selectivity for the rate of frequency modulated (FM) sweeps in the auditory cortex of anesthetized C57bl/6 (C57) mice. Linear downward FM sweeps with rates between 0.08 and 20 kHz/ms were tested. We show that at least two different response properties predict FM rate selectivity: sideband inhibition and duration tuning. Sideband inhibition was determined using the two-tone inhibition paradigm in which excitatory and inhibitory tones were presented with different delays. Sideband inhibition was present in the majority (88%, n = 53) of neurons. The spectrotemporal properties of sideband inhibition predicted rate selectivity and exclusion of the sideband from the sweep reduced/eliminated rate tuning. The second property predictive of sweep rate selectivity was duration tuning for tones. Theoretically, if a neuron is selective for the duration that a sweep spends in the excitatory frequency tuning curve, then rate selectivity will ensue. Duration tuning for excitatory tones was present and predicted rate selectivity in ∼34% of neurons (n = 97). Both sideband inhibition and duration tuning predicted rate selectivity equally well, but sideband inhibition was present in a larger percentage of neurons suggesting that it is the dominant mechanism in the C57 mouse auditory cortex. Similar mechanisms shape sweep rate selectivity in the auditory system of bats and mice and movement-velocity selectivity in the visual system, suggesting similar solutions to analogous problems across sensory systems. This study provides baseline data on basic spectrotemporal processing in the C57 strain for elucidation of changes that occur in presbycusis.

Effects of sound intensity on temporal properties of inhibition in the pallid bat auditory cortex

Auditory neurons in bats that use frequency modulated (FM) sweeps for echolocation are selective for the behaviorally-relevant rates and direction of frequency change. Such selectivity arises through spectrotemporal interactions between excitatory and inhibitory components of the receptive field. In the pallid bat auditory system, the relationship between FM sweep direction/rate selectivity and spectral and temporal properties of sideband inhibition have been characterized. Of note is the temporal asymmetry in sideband inhibition, with low-frequency inhibition (LFI) exhibiting faster arrival times compared to high-frequency inhibition (HFI). Using the two-tone inhibition over time (TTI) stimulus paradigm, this study investigated the interactions between two sound parameters in shaping sideband inhibition: intensity and time. Specifically, the impact of changing relative intensities of the excitatory and inhibitory tones on arrival time of inhibition was studied. Using this stimulation paradigm, single unit data from the auditory cortex of pentobarbital-anesthetized cortex show that the threshold for LFI is on average ~8 dB lower than HFI. For equal intensity tones near threshold, LFI is stronger than HFI. When the inhibitory tone intensity is increased further from threshold, the strength asymmetry decreased. The temporal asymmetry in LFI vs. HFI arrival time is strongest when the excitatory and inhibitory tones are of equal intensities or if excitatory tone is louder. As inhibitory tone intensity is increased, temporal asymmetry decreased suggesting that the relative magnitude of excitatory and inhibitory inputs shape arrival time of inhibition and FM sweep rate and direction selectivity. Given that most FM bats use downward sweeps as echolocation calls, a similar asymmetry in threshold and strength of LFI vs. HFI may be a general adaptation to enhance direction selectivity while maintaining sweep-rate selective responses to downward sweeps.

Mechanisms underlying intensity-dependent changes in cortical selectivity for frequency-modulated sweeps

Frequency-modulated (FM) sweeps are common components of species-specific vocalizations. The intensity of FM sweeps can cover a wide range in the natural environment, but whether intensity affects neural selectivity for FM sweeps is unclear. Bats, such as the pallid bat, which use FM sweeps for echolocation, are suited to address this issue, because the intensity of echoes will vary with target distance. In this study, FM sweep rate selectivity of pallid bat auditory cortex neurons was measured using downward sweeps at different intensities. Neurons became more selective for FM sweep rates present in the bat's echolocation calls as intensity increased. Increased selectivity resulted from stronger inhibition of responses to slower sweep rates. The timing and bandwidth of inhibition generated by frequencies on the high side of the excitatory tuning curve [sideband high-frequency inhibition (HFI)] shape rate selectivity in cortical neurons in the pallid bat. To determine whether intensity-dependent changes in FM rate selectivity were due to altered inhibition, the timing and bandwidth of HFI were quantified at multiple intensities using the two-tone inhibition paradigm. HFI arrived faster relative to excitation as sound intensity increased. The bandwidth of HFI also increased with intensity. The changes in HFI predicted intensity-dependent changes in FM rate selectivity. These data suggest that neural selectivity for a sweep parameter is not static but shifts with intensity due to changes in properties of sideband inhibition.

Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

Multiple mechanisms have been shown to shape frequency-modulated (FM) selectivity within the central nucleus of the inferior colliculus (IC) in the pallid bat. In this study we focus on the mechanisms associated with sideband inhibition. The relative arrival time of inhibition compared with excitation can be used to predict FM responses as measured with a two-tone inhibition paradigm. An early-arriving low-frequency inhibition (LFI) prevents responses to upward sweeps and thus shapes direction selectivity. A late-arriving high-frequency inhibition (HFI) suppresses slow FM sweeps and thus shapes rate selectivity for downward sweeps. Iontophoretic application of gabazine (GBZ) to block GABA(A) receptors or strychnine (Strych) to block glycine receptors was used to assess the effects of removal of inhibition on each form of FM selectivity. GBZ and Strych had a similar effect on FM direction selectivity, reducing selectivity in up to 86% of neurons when both drugs were coapplied. FM rate selectivity was more resistant to drug application with less than 38% of neurons affected. In addition, only Strych could eliminate FM rate selectivity, whereas GBZ alone was ineffective. The loss of FM selectivity was directly correlated to a loss of the respective inhibitory sideband that shapes that form of selectivity. The elimination of LFI correlated to a loss of FM direction selectivity, whereas elimination of HFI correlated to a loss of FM rate selectivity. Results indicate that 1) although the majority of FM direction selectivity is created within the IC, the majority of rate selectivity is inherited from lower levels of the auditory system, 2) a loss of LFI corresponds to a loss of FM direction selectivity and is created through either GABAergic or glycinergic input, and 3) a loss of HFI corresponds to a loss of FM rate selectivity and is created mainly through glycinergic input.

Multiple mechanisms shape selectivity for FM sweep rate and direction in the pallid bat inferior colliculus and auditory cortex

The inferior colliculus and auditory cortex of the pallid bat contain a large percentage of neurons that are highly selective for the direction and rate of the downward frequency modulated (FM) sweep of the bat's echolocation pulse. Approximately 25% of neurons tuned to the echolocation pulse respond exclusively to downward FM sweeps. This review focuses on the finding that this selectivity is generated by multiple mechanisms that may act alone or in concert. In the inferior colliculus, selectivity for sweep rate is shaped by at least three mechanisms: shortpass or bandpass tuning for signal duration, delayed high-frequency inhibition that prevents responses to slow sweep rates, and asymmetrical facilitation that occurs only when two tones are presented at appropriate delays. When acting alone, the three mechanisms can produce essentially identical rate selectivity. Direction selectivity can be produced by two mechanisms: an early low-frequency inhibition that prevents responses to upward sweeps, and the same asymmetrical two-tone inhibition that shapes rate tuning. All mechanisms except duration tuning are also present in the auditory cortex. Discussion centers on whether these mechanisms are redundant or complementary.

Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Inferior Colliculus of the Pallid Bat

This study describes mechanisms that underlie neuronal selectivity for the direction and rate of frequency-modulated sweeps in the central nucleus of the inferior colliculus (ICC) of the pallid bat (Antrozous pallidus). This ICC contains a high percentage of neurons (66%) that respond selectively to the downward sweep direction of the bat's echolocation pulse. Some (19%) are specialists that respond only to downward sweeps. Most neurons (83%) are also tuned to sweep rates. A two-tone inhibition paradigm was used to describe inhibitory mechanisms that shape selectivity for sweep direction and rate. Two different mechanisms can create similar rate tuning. The first is an early on-best frequency inhibition that shapes duration tuning, which in turn determines rate tuning. In most neurons that are not duration tuned, a delayed high-frequency inhibition creates rate tuning. These neurons respond to fast sweep rates, but are inhibited as rate slows, and delayed inhibition overlaps excitation. In these neurons, starting a downward sweep within the excitatory tuning curve eliminates rate tuning. However, if rate tuning is shaped by duration tuning, this manipulation has no effect. Selectivity for the downward sweep direction is created by an early low-frequency inhibition that prevents responses to upward sweeps. In addition to this asymmetry in arrival times of low- and high-frequency inhibitions, the bandwidth of the low-frequency sideband was broader. Bandwidth influences the arrival time of inhibition during an FM sweep because a broader sideband will be encountered sooner. These findings show that similar spectrotemporal filters can be created by different mechanisms.

Inhibitory and excitatory response areas of neurons in the central nucleus of the inferior colliculus in unanesthetized chinchillas

In unanesthetized chinchillas, we determined excitatory and inhibitory response regions of neurons in the central nucleus of the inferior colliculus (ICc). The responses of 250 multiunits and 47 single units in the ICc to one- and two-tone stimuli were measured by extracellular recordings. The one-tone excitatory response area of ICc neurons from awake chinchillas was classified as either narrow with a steep high-frequency slope >140 dB/oct (type 1), broad with a high-frequency slope <140 dB/oct (type 2), or complex with a negative high-frequency slope (type 3). One-tone inhibition was prominent only in units with a high spontaneous firing rate. As revealed with two-tone stimuli, inhibition in the ICc of awake chinchillas and its relation to excitatory response regions was different from what is reported in anesthetized animals. The two-tone inhibitory responses were classified as follows: (1) inhibitory regions of equal strength on both sides of the characteristic frequency; (2) asymmetrical inhibitory regions, more prominent at the high-frequency side of the characteristic frequency; (3) strong inhibitory regions overlying most of the one-tone excitatory response region; (4) inhibitory response regions lying only within the one-tone excitatory response region; and (5) neurons without clear two-tone inhibition. One-tone and two-tone inhibitory regions of the same unit were markedly different in 66% of the units with a high spontaneous rate. The neural response to frequencies within the inhibitory regions often was an onset response followed by inhibition. Excitatory and inhibitory response properties were similar over considerable penetration distances (600-1,000 microm) in a particular dorso-ventral recording track.

Spectral shape sensitivity contributes to the azimuth tuning of neurons in the cat's inferior colliculus.

We recorded high-best-frequency single-unit responses to free-field noise bursts that varied in intensity and azimuth to determine whether inferior colliculus (IC) neurons derive directionality from monaural spectral-shape. Sixty-nine percent of the sample was directional (much more responsive at some azimuths than others). One hundred twenty-nine directional units were recorded under monaural conditions (unilateral ear plugging). Binaural directional (BD) cells showed weak monaural directionality. Monaural directional (MD) cells showed strong monaural directionality, i.e., were much more responsive at some directions than others. Some MD cells were sensitive to both monaural and binaural directional cues. MD cells were monaurally nondirectional in response to tone bursts that lack direction-dependent variation in spectral shape. MD cells were unresponsive to noise bursts at certain azimuths even at high intensities showing that particular spectral shapes inhibit their responses. Two-tone inhibition was stronger where MD cells were unresponsive to noise stimulation than at directions where they were responsive. According to the side-band inhibition model, MD cells derive monaural directionality by comparing energy in excitatory and inhibitory frequency domains and thus should have stronger inhibitory side-bands than BD cells. MD and BD cells showed differences in breadth of excitatory frequency domains, strength of nonmonotonic level tuning, and responsiveness to tones and noise that were consistent with this prediction. Comparison of these data with previous findings shows that strength of spectral inhibition increases greatly between the level of the cochlear nucleus and the IC, and there is relatively little change in strength of spectral inhibition among the IC, auditory thalamus, and cortex.

Corticofugal modulation of frequency tuning of inferior collicular neurons in big brown bat,Eptesicus fuscus

In order to explore the possible mechanism of corticofugal modulation of excitatory frequency tuning curves (EFTCs) of midbrain neurons, we examined the change of sharpness, frequency-intensity response area, minimum threshold of both EFTCs and inhibitory frequency tuning curves (IFTCs) of inferior collicular neurons during corticofugal modulation using two-tone inhibition paradigm and micro-electrical stimulation technique. Our data showed that corticofugal inhibition increased sharpness, minimum threshold, and decreased the frequency-intensity response area of EFTCs, at the same time it decreased the sharpness, minimum threshold but increased the frequency-intensity response area of IFTCs. The opposite results were observed for EFTCs and IFTCs of corticofugally facilitated inferior collicular neurons. During corticofugal inhibition, the percent change of frequency-intensity response area of EFTCs had significant correlation with the percent change of that of IFTCs. These data suggest that cortical neurons are likely to improve frequency information processing of inferior collicular neurons by modulation of IFTCs.

Neural inhibition sharpens auditory spatial selectivity of bat inferior collicular neurons.

This study examines the role of neural inhibition in auditory spatial selectivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, using a two-tone inhibition paradigm. Two-tone inhibition decreases auditory spatial response areas but increases the slopes of directional sensitivity curves of inferior collicular neurons. Inferior collicular neurons have either directionally-selective or hemifield directional sensitivity curves. A directionally-selective curve always has a peak which is at least 50% larger than the minimum. A hemifield directional sensitivity curve rises from an ipsilateral angle by more than 50% and either reaches a plateau or declines by less than 50% over a range of contralateral angles. Two-tone inhibition does not change directionally-selective curves but changes most hemifield directional sensitivity curves into directionally-selective curves. Auditory spatial selectivity determined both with and without two-tone inhibition increases with increasing best-excitatory frequency. Sharpening of auditory spatial selectivity by two-tone inhibition is larger for neurons with smaller differences between excitatory and inhibitory best frequencies. The effect of two-tone inhibition on auditory spatial selectivity increases with increasing inhibitory tone intensity but decreases with increasing intertone interval. The implications of these findings in bat echolocation are discussed.

Corticofugal regulation of excitatory and inhibitory frequency tuning curves of bat inferior collicular neurons

Corticofugal regulation of excitatory and inhibitory frequency tuning curves (FTCs) of neurons in the central nucleus of bat inferior colliculus (ICc) was studied by electrical stimulation of the primary auditory cortex (AC stimulation) under free field stimulation conditions using a two-tone inhibition paradigm. AC stimulation narrowed the excitatory FTCs and asymmetrically expanded the lateral inhibitory FTCs of corticofugally inhibited ICc neurons. The opposite results were observed for excitatory and inhibitory FTCs of corticofugally facilitated ICc neurons. These data support previous reports that corticofugal systems work together with widespread lateral inhibition to regulate subcortical frequency processing.

Monaural spectral contrast mechanism for neural sensitivity to sound direction in the medial geniculate body of the cat.

Monaural spectral contrast mechanism for neural sensitivity to sound direction in the medial geniculate body of the cat. J. Neurophysiol. 78: 2754-2771, 1997. Central auditory neurons vary in sound direction sensitivity. Insensitive cells discharge well to all sound source directions, whereas sensitive cells discharge well to certain directions and poorly to others. High-frequency neurons in the latter group are differentially sensitive to binaural and monaural directional cues present in broadband noise (BBN). Binaural directional (BD) cells require binaural stimulation for directional sensitivity; monaural directional (MD) cells are sensitive to the direction of monaural stimuli. A model of MD sensitivity was tested using single-unit responses. The model assumes that MD cells derive directional sensitivity from pinna-derived spectral cues (head related transfer function, HRTF). This assumption was supported by the similarity of effects that pinna orientation produces on locations of HRTF patterns and on locations of MD cell azimuth function peaks and nulls. According to the model, MD neurons derive directional sensitivity by use of excitatory/inhibitory antagonism to compare sound pressure in excitatory and inhibitory frequency domains, and a variety of observations are consistent with this idea. 1) Frequency response areas of MD cells consist of excitatory and inhibitory domains. MD cells exhibited a higher proportion of multiple excitatory domains and narrower excitatory frequency domains than BD cells, features that may reflect specialization for spectral-dependent directional sensitivity. 2) MD sensitivity requires sound pressure in excitatory and inhibitory frequency domains. Directional sensitivity was evaluated using stimuli with frequency components confined exclusively to excitatory domains (E-only stimuli) or distributed in both excitatory and inhibitory domains (E/I stimuli). Each of 13 MD cells that were tested exhibited higher directional sensitivity to E/I than to E-only stimuli; most MD cells exhibited relatively low directional sensitivity when frequency components were confined exclusively to excitatory domains. 3) MD sensitivity derives from excitatory/inhibitory antagonism (spectral inhibition). Comparison of responses to best frequency and E/I stimuli provided strong support for spectral inhibition. Although spectral facilitation conceivably could contribute to directional sensitivity with direction-dependent increases in response, the results did not show this to be a significant factor. 4) Direction-dependent decreases in responsiveness to BBN reflect increased sound pressure in inhibitory relative to excitatory frequency domains. This idea was tested using the strength of two-tone inhibition, which is a function of stimulus levels in inhibitory relative to excitatory frequency domains. The finding that two-tone inhibition was stronger at directions where BBN responses were minimal than at directions where they were maximal supports the model.

Physiology and tonotopic organization of auditory receptors in the cricket Gryllus bimaculatus DeGeer.

Physiological recordings were obtained from identified receptors in the tympanal organ of Gryllus bimaculatus. By immersing the prothoracic leg in Ringer solution and removing the anterior tympanic membrane the auditory receptors were exposed without significantly altering the frequency response of the auditory organ (Fig. 1). Each receptor was tuned to a specific sound frequency. For sound frequencies below this characteristic frequency the roll-off in sensitivity decreased from 20-30 dB/octave to 10-15 dB/octave as the characteristic frequency of receptors increased from 3-11 kHz (Fig. 4A). For each individual receptor the slope, dynamic range and maximum spike response were similar for different sound frequencies (Fig. 9A). The receptors were tonotopically organized with the characteristic frequency of the receptors increasing from the proximal to the distal end of the array (Figs. 5, 6). Several receptors had characteristic frequencies of 5 kHz. These receptors were divided into two groups on the basis of their maximum spike response produced in response to pure tones of increasing intensity (Fig. 7). Independent of the tuning of the receptor no two-tone inhibition was observed in the periphery, thus confirming that such interactions are a property of central integration.

The role of two-tone suppression in song coding by ventral cord neurones in the cricketTeleogryllus oceanicus (Le Guillou)

1. The calling, courtship and aggression songs ofT. oceanicus have distinctive temporal patterns but their spectral compositions are very similar: the carrier frequency occurs around 4.5 kHz and harmonics occur which extend above background noise level up to at least 40 kHz (Fig. 1). 2. Units were recorded in the cervical connectives which responded to sound frequencies over the range from 1 kHz to at least 40 kHz. The sensitivities of some of the high frequency units were comparable to, or exceeded, the sensitivities of the units responding to the carrier frequencies of the species songs (Fig. 2). 3. At the level of the neck connectives, units responding to the range from 10 kHz to 40 kHz could be divided, on the basis of their prothoracic morphology and physiology, into Through Neurones and Ascending Neurones. All the recorded neurones showed two-tone suppression effects but they varied in their degree of susceptibility to suppression. Frequencies in the range 4–5 kHz were most effective in producing suppression of the responses to high frequency tones (Figs. 5, 6). 4. The two identified Ascending Neurone types had similar morphologies in the prothoracic ganglion (Fig. 3). ANA showed tonic responses to pure tones in the frequency range from 10 kHz to 40 kHz. Below 10 kHz high intensity inhibition of the response occurred and the latency increased from about 15 ms for an 18 kHz tone pulse, to about 55 ms for a 4.5 kHz tone (Fig. 4). ANB responded with 1–3 spikes to stimuli in the frequency range from 7 kHz to 40 kHz. The response latency to an 18 kHz tone pulse was about 15 ms. No responses were obtained to 50 ms stimuli in the range from 2 kHz to 7 kHz (Fig. 6). However, considerable rebound activity was produced in response to 4.5 kHz stimuli of 200 ms or more; the latency of the rebound to 200 ms stimuli was about 400 ms (Fig. 6C). 5. ANA neurones responded to the syllables of the natural songs (Fig. 7), clearly coding the temporal patterns of the three songs. Cutting the contralateral leg nerve resulted in no detectable change in the neurone's response pattern. ANB neurones responded only during the intervals between chirps and during pauses within chirps. A long period of bursting activity occurred at the end of each song sequence (i.e. 3 chirps). This rebound activity may be the result of extreme inhibition caused by the CF of the songs (Fig. 7). 6. Synthesised natural songs (Fig. 1 E) with the correct temporal parameters but filled with 4.5 kHz alone, 18 kHz alone or a combination of 18 kHz and 4.5 kHz, were produced to investigate the role of two-tone suppression phenomena in song coding. The responses of both ANA and ANB (Fig. 8) showed the interaction of excitatory and inhibitory inputs to these units during the coding of the species songs. 7. Two-tone inhibition effects are advanced as the basic mechanism for the accurate coding of temporal characteristics in the songs ofT. oceanicus. Two different strategies for the recognition of species song types in crickets are advanced.

Frequency selectivity in the anuran medulla: Excitatory and inhibitory tuning properties of single neurons in the dorsal medullary and superior olivary nuclei

1. The excitatory and inhibitory tuning properties of 70 dorsal medullary nucleus (DMN) and 108 superior olivary nucleus (SON) neurons were examined in the medulla of the northern leopard frog (Rana p. pipiens). Inhibitory tuning curves were determined using the two-tone inhibition (TTI) paradigm. 2. The tuning properties of DMN neurons were very similar to those of the VIIIth nerve fibers. (1) Excitatory tuning curves were unimodal, (2) only low frequency (80–500 Hz) tuned neurons exhibited TTI, (3) only higher frequencies were inhibitory, and (4) relative inhibitory thresholds were dependent upon the intensity of the excitatory tone (i.e., as the excitatory tone intensity was elevated, so was the inhibitory threshold). Also like VIIIth nerve fibers, most DMN neurons responded tonically to tonal stimulation. Unlike VIIIth nerve fibers, a small percentage (11%) of DMN neurons elicited a phasic-on response to tonal stimulation. 3. Most SON neurons also exhibited excitatory and inhibitory tuning properties similar to those of the VIIIth nerve. However, 19% exhibited properties previously reported only at the midbrain level of the auditory system. These latter properties include (1) bimodal, recurved and closed excitatory tuning curve configurations; (2) all neurons, not just those tuned to low frequencies, were susceptible to TTI; (3) TTI was exerted by lower, as well as higher, frequencies, and (4) TTI thresholds could be independent, as well as dependent, upon the intensity of the excitatory tone. Also like midbrain neurons, a small percentage (4%) of SON neurons exhibited a phasic-off response to tonal stimulation. 4. In both the DMN and SON, some neurons exhibited the ability to respond consecutively to tone cycles, trill pulses and beats generated by 2 tones at repetition rates up to 280 Hz. The maximum following rate of a given neuron was similar for each type of repeating event. Neurons tuned to all frequency ranges exhibited this property, and all acted as low-pass temporal filters.

Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior

1. In the cricket,Teleogryllus oceanicns, an identified auditory interneuron, interneuron-1 (int-1), is described morphologically and physiologically (Figs. 1,2). There is one such neuron in each hemiganglion of the prothoracic ganglion. The medial dendrites of int-1 overlap part of the terminal field formed by the auditory afferent axons from the ear and int-1's axon ascends to the brain, terminating on the same (ipsilateral) side (Fig- 2). 2. The neuron has a two-part frequency response characteristic: (1) its spontaneous activity is suppressed by low frequencies (3 to 8 kHz) at threshold-to-moderate intensities (Fig. 9 B), and (2) it is strongly excited at high frequencies, especially ultrasonic, from 15–100 kHz (Fig. 3). 3. Int-1 produces more spikes per tone pulse (Fig. 4) and its reponse latency decreases (Fig. 5), with increasing levels of intensity when stimulated by ultrasound. 4. Two-tone inhibition occurs in int-1. When a 30 kHz (normally excitatory) tone is combined with a 5 kHz tone (which suppresses spontaneous activity), the combination tone results in a diminished response, compared to the response to the excitatory tone alone (Fig. 6). 5. The excitation of int-1 shows lateralization. Excitation is stronger in the neuron ipsilateral to the sound source, than in the contralateral int-1 (Fig. 9). 6. Int-1 responds to electronically-generated pulse trains that simulate bat-echolocation signals. The neuron is responsive to a range of ultrasonic frequencies that are contained in the echolocation signals of insectivorous bats (Fig. 11). 7. In light of its response characteristics, we speculate that int-1 plays a role in the detection of ultrasonic signals emitted in the cricket's normal environment by hunting bats.

Frequency selectivity in the anuran auditory midbrain: Single unit responses to single and multiple tone stimulation

1. The excitatory response properties of 130 single units in the torus semicircularis of the northern leopard frog (Rana p, pipiens) were recorded. 86% responded maximally to single tones. 14% responded maximally only to specific combinations of 2 or more tones, and were either completely unresponsive or weakly responsive (<20% maximal response) to single tones over a wide range of intensities. 2. Single tone responders were placed in 6 classes on the basis of configurations of their excitatory tuning curves. Neurons in each class also tended to show similar inhibitory response properties, particularly in regard to exhibiting partial or total two-tone inhibition (TTI). Neurons with symmetrical excitatory tuning curves generally exhibited only partial TTI, while those with more asymmetrical curves exhibited total TTI. 3. Inhibitory response properties were determined for 78 single tone responders. 69% could be totally inhibited by a second tone; the remainder showed only partial two-tone inhibition (TTI). Most neurons exhibiting total TTI (74%) had best inhibitory frequencies (BIFs) which were lower than the best excitatory frequencies (BEFs). Only 26% had BIFs > BEFs. 4. Absolute thresholds for total TTI by frequencies lower than the BEF were sometimes independent of the intensity of the excitatory tone. The property was not observed in the absolute thresholds for total TTI by higher frequencies, in which case all inhibitory thresholds were elevated upon increasing the intensity of the excitatory tone. 5. A small number of neurons were either unresponsive or weakly responsive (<20% maximal excitation) to broad-band stimulation. This response property was associated with total TTI in which the relative inhibitory threshold was lower than the intensity of the excitatory tone. 6. Neurons requiring 2 or more tones for maximal excitation all had restricted excitatory frequency bands from which the tone combinations could be drawn. These neurons were placed in two categories: those requiring narrowly separated ( 500 Hz) tones and had two excitatory bands. The latter category required the presence of one tone from each band to be excited. 7. All multiple tone responders could be totally inhibited by the addition of a single tone to the excitatory tone combination. Also, all multiple tone responders had non-monotonic intensity-rate functions, with excitatory intensity ranges as narrow as 25 dB and as broad as 50 dB. 8. The frequency selectivities of all multiple tone responders matched the spectral features of the species mating call. Their possible role in the selective detection of this call is discussed.

Some Perceptual Aspects of Timbre

In the study of how we perceive musical timbre, we encounter a number of different representations of the musical information, several of which have appeared in preceding papers in the symposium. The first is the musical score, which in engineering terms is a graph of frequency versus time, with appended annotations about loudness, scoring, timing, etc. The next representation is sound in a concert hall, created from the score by an orchestra or computer: technically, sound pressure as a function of time. The representations of interest in this paper are those produced by the mechanical and neural systems in our heads in response to this sound. The First Auditory Representation Properties of the Ear Experiments involving auditory masking (see Patterson 1976), critical bands (summarized in Tobias 1970), basilar membrane motion (see Johnstone & Boyle 1967; Rhode 1971; & Evans & Wilson 1973) and tuning curves of primary auditory nerve fibers (see Kiang 1965 & 1974), all indicate that the first neural representation of sound in our heads results from a frequency analysis of the incoming sound by a fluid-filled bony structure called the cochlea. The frequency resolution of this system is somewhat less than one-third of an octave (above 400 Hz), as can be seen from Figure 1, the so-called critical bandwidth data derived from psychophysics. A corresponding set of psychophysical experiments indicate that the temporal resolution of the system is at best a few milliseconds (e.g., see Viemeister 1979). The phase sensitivity of the is still a contro versial topic, but most studies indicate that the system is only minimally sensitive to the relative phase of harmonics. Of course, the is exquisitely sensitive to the interaural phase of any sine wave component below 500 Hz. But this gives rise to auditory localization, and not perception of timbre. Hence in the remainder of this paper we will ignore phase. It may at first glance seem quite incongruous that the auditory system, which has excellent pitch discrimination (two or three hertz for 1000 Hz pure tones), should analyze sound with filters as broad as one third of an octave, that is, three or four notes on the chromatic scale. But it is easy to show that if one uses not just one filter, but several overlapping filters, then accurate information concerning pitch is available, limited only by the slope of the filter characteristic, and not the filter bandwidth. The Model To obtain a better idea of this first neural representation of music and speech, we have constructed a model ear with properties approximating those of the human discussed above. Our model, shown in Figure 2, consists basically of a bank of 1/3 octave filters, covering from 125 Hz to 6.3 kHz, followed by envelope detectors. To simulate the roughly constant critical bandwidth below 400 Hz, we added together the detector outputs of the 125- and 160-Hz channels, and also the 200- and 250-Hz channels (see Dockendorff 1978). The detector time constants were chosen to produce fast rise time consistent with low ripple. In filter systems such as this one which have wider band widths at higher frequencies, the rise time of the filters decrease with increasing cent er frequency. Hence we chose detector time constants to correspond, such that the overall rise times of the filter-detector units were inversely proportional to frequency. Specifically, the 1 kHz channel has an overall rise time of 6 milliseconds, the 2 kHz channel, 3 milliseconds, and so forth. As noted in Figure 2, the detectors are connected to a 16-channel CMOS multiplex switch, which samples the output of each channel every 1.6 milliseconds. (This rate is appropriate for the high-frequency channels, but oversamples the low channels.) The multiplexed output is then passed through a logarithmic amplifier to match the logarithmic nature of perceived loudness in the ear. There are several important aspects of the human auditory system that are not modeled by this system, such as two-tone inhibition, the limited dynamic range of the neural system, etc. …

Detection of tones in band-reject noise.

Three experiments were conducted to investigate the detectability of tonal signals simultaneously presented with computer-generated, long duration (.5 sec), band-reject maskers. In Experiment 1, detectability of a tone of 500, 1000, or 2000 Hz presented at 50 dB SPL was measured as a function of the width of a spectral "notch" symmetrically placed around the tone. A narrow notch resulted in decreased detectability relative to the wide band (zero-notch width) control condition. Further increases in notch width resulted in increased detectability until subjects approached errorless performance. In Experiment 2, psychometric functions were obtained for a 1000-Hz tone presented in four notch-noise conditions. The slopes of the psychometric functions were consistently steeper in the band-reject conditions relative to the zero notch-width condition. These slope differences result in relationships between threshold and notch width that depend upon the region of the psychometric function from which the threshold estimates are obtained. In Experiment 3, the decrease in performance associated with the notch was found to increase in proportion to notch depth. The data suggest that spectral edges placed in the immediate vicinity of a tone reduce the detectability of the tonal signal. This "edge effect" is discussed in relation to two-tone inhibition that has been observed in the auditory nerve.

Post-Metamorphic Development of the Frequency Selectivities and Sensitivities of the Peripheral Auditory System of the Bullfrog, Rana Catesbeiana

ABSTRACT Acoustic response characteristics of single fibres were studied in the VIIIth cranial nerve of adult and early post-metamorphic bullfrogs (Rana catesbeiana). Based on the distribution of units’ best excitatory frequencies, three populations of auditory fibres were found in each group of frogs. The sharpness of the tuning curves and temporal firing patterns of primary fibres were similar in both adults and froglets. However, the distributions of the populations were different between the two groups, and it was found that froglets responded to higher frequencies than did adults. There were also differences in the distributions of thresholds of excitation between the froglets and adults. The excitation thresholds of low-frequency selective and high-frequency selective fibres tended to be higher in froglets. Low-frequency selective fibres in both groups of frogs exhibited two-tone inhibition, and the best inhibitory frequencies were higher in froglets than in adults. These results demonstrate that changes in the response properties of primary auditory fibres occur during the development of the bullfrog. These functional changes presumably reflect morphological changes which may occur in the peripheral auditory system.