Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog,Hyla cinerea

Summary Twenty four castrated male, 6 intact male, and 11 intact female Hyla cinerea were injected subcutaneously with 25 g arginine-vasotocin (AVT) and induced to call 1 h later in response to the playback of a conspecific mating call. Eighteen castrated males and 8 intact females were implanted 5 mg androgen pellets for 3 weeks prior to the neuropeptide injection. Among castrated males, 6/9 testosterone (T) implanted, 4/9 dihydrotestosterone (DHT) implanted and 2/6 non implanted individuals produced calls after being administered AVT. 5/6 intact non implanted males and 6/8 T intact implanted females also called, and 3 intact non implanted females remained silent after the injection. Evoked calls had a mid-frequency spectral peak at about 1900 Hz which is absent in field-recorded mating calls of this species. Calls of implanted females and castrated non implanted males were shorter than those of castrated implanted and intact non implanted males. Audiograms measured before hormone implants showed dips of enhanced sensitivity at about 0.5, 0.9 and 3.0 kHz in males and females. After AVT injection, thresholds at frequencies within the 0.7–1.5 kHz range were increased in castrated males. Such reduction in sensitivity points to an inhibition of the auditory system during hormone induced vocal activation.Abbreviations AVT arginine-vasotocin - DHT dihydrotestosterone - T testosterone - TS torus semicircularis     

Acoustic response properties of single units in the torus semicircularis of the goldfish,Carassius auratus

Single units of the goldfish torus semicircularis (TS) were recorded in response to pure tones. Response areas (RA) were obtained by recording the number of spikes evoked by tones in a range of frequencies and levels within the units' dynamic range. RAs gave estimates of best sensitivity (BS), characteristic frequency (CF), most excitatory frequency at each level (BF), and Q_10dB. Peri-stimulus-time histograms (PSTH), interspike interval histograms (ISIH), and period histograms were obtained at various frequencies and levels to describe the units' temporal response patterns.The distribution of CF is nonuniform with modes at 155, 455, and 855 Hz. The distribution of the coefficient of synchronization to standard tones is also nonuniform, revealing a dichotomy between units with little or no phase-locking and those that phase-lock strongly. PSTHs for units without significant phase-locking vary widely and include patterns resembling those of the mammalian auditory brainstem. Compared with saccular afferents, torus units tend to have lower spontaneous rates, greater sensitivity, and sharper tuning. Unlike saccular afferents, BF is independent of level for most torus units. Some torus units are similar to saccular afferents while others reveal significant transformations of information between the periphery and the midbrain.Abbreviations BF best frequency - BS best sensitivity - CF characteristic frequency - ISIH inter-spike interval histogram - PSTH peri-stimulus-time histogram - RA response area - TS torus semicircularis     

Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish,Eigenmannia

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13–18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10–20 Hz) at a total length of 25–30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pacemaker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18. Within the torus semicircularis, giant cells are necessary for the performance of the JAR. Giant cell numbers increase exponentially during development and the onset of the JAR coincides with a minimum of at least 150 giant cells and the attainment of a total length of at least 15 mm and at least 150 giant cells. Pacemaker and relay cells comprise the adult Eigenmannia pacemaker nucleus. The growth and differentiation of these cell types also correlates with the onset of the JAR in developing animals. We describe a gradual improvement of sensory abilities, as opposed to an explosive onset of the mature JAR. We further suggest that this may be a rule common in most developing behavioral systems. © 1992 John Wiley & Sons, Inc.     

Dissimilarities in auditory tuning in midwife toads of the genus Alytes (Amphibia: Anura)

The auditory sensitivity in three species of the anuran genus Alytes (Alytidae) was examined to determine patterns of intra‐ and interspecific variation, relating these measurements to behavioural preferences measured in previous studies and to the adaptive and evolutionary significance of this sensory function. The audiograms obtained with multi‐unit recordings in the torus semicircularis of 13 Alytes cisternasii, 10 Alytes obstetricans, and eight Alytes dickhilleni show two regions of enhanced sensitivity, between approximately 100–500 and 1200–2400 Hz, with minimum thresholds at approximately 40 and 45 dB SPL, respectively. The mean and range of the high‐frequency region differed among species, although the sensitivity, measured as minimum thresholds, was similar. The region of high‐frequency sensitivity was centred at approximately the frequency of the advertisement call in A. cisternasii but, in A. obstetricans and A. dickhilleni, was centred at frequencies higher than the conspecific calls. These results contrast with preferences for lower frequencies exhibited by Alytes in female phonotactic and in male evoked vocal responses. Such loose relationships between signals and receivers suggest that the divergence of the sound communication system in Alytes has implied environmental and phylogenetic factors in addition to sexual selection processes.     

Midbrain auditory sensitivity in the spring peeper (Pseudacris crucifer): correlations with behavioral studies

1. We derived audiograms from recordings of multiunit activity in the torus semicircularis of 10 males and 6 females of the spring peeper from central Missouri, USA. We used free-field stimulation with tone bursts that had temporal properties similar to typical advertisement calls and that ranged in frequency from 500-6000 Hz. 2. Audiograms from different electrode positions in the same animal had the same general shape. There was no evidence of tonotopy. 3. Audiograms showed two regions of maximal sensitivity: a low-frequency region (500-700 Hz); and a high-frequency region (2000-4000 Hz). Absolute thresholds and frequencies of maximum sensitivity varied considerably from individual to individual. 4. Audiograms derived from all individuals of each sex indicated that in the high-frequency region, corresponding to the frequency range of advertisement calls, males were more broadly tuned than females. However, tuning in both sexes was relatively weak, and the data predict relatively little selectivity in behavioral responses over the entire range of variation in frequency of the advertisement call in local populations. 5. The results are discussed in terms of behavioral experiments with both males and females from the same populations in central Missouri. We show that merely summarizing the audiograms based on estimates of minimum thresholds of a population or species may mask significant individual differences in tuning. Moreover, most behavioral studies are conducted at playback levels considerably above threshold. For these reasons, behavioral selectivity is not always accurately predicted by inspection of "average" audiograms.     

Interval-integration underlies amplitude modulation band-suppression selectivity in the anuran midbrain

We examined the mechanisms that underlie band-suppression amplitude modulation selectivity in the auditory midbrain of anurans. Band-suppression neurons respond well to low (5–10 Hz) and high (>70 Hz) rates of sinusoidal amplitude modulation, but poorly, if at all, to intermediate rates. The effectiveness of slow rates of sinusoidal amplitude modulation is due to the long duration of individual pulses; short-duration pulses (<10 ms) failed to elicit spikes when presented at 5–10 pulses s^–1. Each unit responded only after a threshold number of pulses (median=3, range=2–5) were delivered at an optimal rate. The salient stimulus feature was the number of consecutive interpulse intervals that were within a cell-specific tolerance. This interval-integrating process could be reset by a single long interval, even if preceded by a suprathreshold number of intervals. These findings indicate that band-suppression units are a subset of interval-integrating neurons. Band-suppression neurons differed from band-pass interval-integrating cells in having lower interval-number thresholds and broader interval tolerance. We suggest that these properties increase the probability of a postsynaptic spike, given a particular temporal pattern of afferent action potentials in response to long-duration pulses, i.e., predispose them to respond to slow rates of amplitude modulation. Modeling evidence is provided that supports this conclusion.Abbreviations AM amplitude modulation - PRR pulse repetition rate - SAM sinusoidal amplitude modulation     

Sharpening of directional responses along the auditory pathway of the oyster toadfish, <Emphasis Type="Italic">Opsanus tau</Emphasis>

Our previous studies have shown that the peripheral auditory system of the toadfish encodes the direction of a sound source. Here, we compare directional responses of peripheral saccular afferents, cells in the descending octaval nucleus (DON) of the medulla, and the torus semicircularis (TS) of the midbrain. Recording locations in the brain were labeled with neurobiotin to confirm the site. To compare directional responses among cells, we calculated an index [sharpening ratio (SR)] that weights the relative strength of responses to the best direction for that cell and to the adjacent stimulus angles tested. Unsharpened saccular afferents tend to have a cosinusoidal directional response pattern (DRP) with an expected SR of 0.87. In DON, more than 60% of the cells exhibited directional sharpening (defined as SR <0.8). In TS, more than 80% of the cells exhibited directional sharpening. We conclude that directional auditory sharpening first occurs in DON and some additional sharpening occurs in the ascending pathway to the midbrain, particularly in azimuth. The sharpening of directional selectivity is likely to be an important component of the neural computations underlying directional hearing.