Responses to simulated echoes by neurons in the barn owl's auditory space map

The natural acoustical environment contains many reflective surfaces that give rise to echoes, complicating the task of sound localization and identification. The barn owl (Tyto alba), as a nocturnal predator, relies heavily on its auditory system for tracking and capturing prey in this highly echoic environment. The external nucleus of the owl's inferior colliculus (ICx) contains a retina-like map of space composed of space-specific auditory neurons that have spatially limited receptive fields. We recorded extracellularly from individual space-specific neurons in an attempt to understand the pattern of activity across the ICx in response to a brief direct sound and a simulated echo. Space-specific neurons responded strongly to the direct sound, but their response to a simulated echo was suppressed, typically, if the echo arrived within 5 ms or less of the direct sound. Thus we expect there to be little or no representation within the ICx of echoes arriving within such short delays.Behavioral tests using the owl's natural tendency to turn their head toward a sound source suggested that owls, like their space-specific neurons, similarly localize only the first of two brief sounds. Naive, untrained owls were presented with a pair of sounds in rapid succession from two horizontally-separated speakers. With interstimulus delays of less than 10 ms, the owl consistently turned its head toward the leading speaker. Longer delays elicited head turns to either speaker with approximately equal frequency and in some cases to both speakers sequentially.Abbreviations IC inferior colliculus - ICx external nucleus of the inferior colliculus - ITD interaural time difference - ISI interstimulus interval - LS left speaker - RS right speaker - CS centering speaker - RF receptive field     

Sensitivity to interaural time difference and representation of azimuth in central nucleus of inferior colliculus in the barn owl

Standard electrophysiology and virtual auditory stimuli were used to investigate the influence of interaural time difference on the azimuthal tuning of neurons in the core and the lateral shell of the central nucleus of the inferior colliculus of the barn owl. The responses of the neurons to virtual azimuthal stimuli depended in a periodic way on azimuth. Fixation of the interaural time difference, while leaving all other spatial cues unchanged, caused a loss of periodicity and a broadening of azimuthal tuning. This effect was studied in more detail in neurons of the core. The azimuthal range tested and the frequency selectivity of the neurons were additional parameters influencing the changes induced by fixating the interaural time difference. The addition of an interaural time difference to the virtual stimuli resulted in a shift of the tuning curves that correlated with the interaural time difference added. In this condition, tuning strength did not change. These results suggest that interaural time difference is an important determinant of azimuthal tuning in all neurons of the core and lateral shell of the central nucleus of the inferior colliculus, and is the only determinant in many of the neurons from the core.     

Pupillary dilation response as an indicator of auditory discrimination in the barn owl

The pupil of an awake, untrained, head-restrained barn owl was found to dilate in response to sounds with a latency of about 25 ms. The magnitude of the dilation scaled with signal-to-noise ratio. The dilation response habituated when a sound was repeated, but recovered when stimulus frequency or location was changed. The magnitude of the recovered response was related to the degree to which habituating and novel stimuli differed and was therefore exploited to measure frequency and spatial discrimination. Frequency discrimination was examined by habituating the response to a reference tone at 3 kHz or 6 kHz and determining the minimum change in frequency required to induce recovery. We observed frequency discrimination of 125 Hz at 3 kHz and 250 Hz at 6 kHz – values comparable to those reported by others using an operant task. Spatial discrimination was assessed by habituating the response to a stimulus from one location and determining the minimum horizontal speaker separation required for recovery. This yielded the first measure of the minimum audible angle in the barn owl: 3° for broadband noise and 4.5° for narrowband noise. The acoustically evoked pupillary dilation is thus a promising indicator of auditory discrimination requiring neither training nor aversive stimuli. Accepted: 28 February 2000     

Passive sound localization of prey by the pallid bat (Antrozous p. pallidus)

Summary The pallid bat (Antrozous p. pallidus) uses passive sound localization to capture terrestrial prey. This study of captive pallid bats examined the roles of echolocation and passive sound localization in prey capture, and focused on their spectral requirements for accurate passive sound localization.Crickets were used as prey throughout these studies. All tests were conducted in dim, red light in an effort to preclude the use of vision. Hunting performance did not differ significantly in red light and total darkness, nor did it differ when visual contrast between the terrestrial prey and the substrate was varied, demonstrating that the bats did not use vision to locate prey.Our bats apparently used echolocation for general orientation, but not to locate prey. They did not increase their pulse emission rate prior to prey capture, suggesting that they were not actively scanning prey. Instead, they required prey-generated sounds for localization. The bats attended to the sound of walking crickets for localization, and also attacked small, inanimate objects dragged across the floor. Stationary and/or anesthetized crickets were ignored, as were crickets walking on substrates that greatly attenuated walking sounds. Cricket communication sounds were not used in prey localization; the bats never captured stationary, calling crickets.The accuracy of their passive sound localization was tested with an open-loop passive sound localization task that required them to land upon an anesthetized cricket tossed on the floor. The impact of a cricket produced a single 10–20 ms duration sound, yet with this information, the bats were able to land within 7.6 cm of the cricket from a maximum distance of 4.9 m. This performance suggests a sound localization accuracy of approximately ±1° in the horizontal and vertical dimensions of auditory space. The lower frequency limit for accurate sound localization was between 3–8 kHz. A physiological survey of frequency representation in the pallid bat inferior colliculus suggests that this lower frequency limit is around 5 kHz.     

Analysis of spectral shape in the barn owl auditory system

In a behavioral experiment, we investigated how efficiently barn owls (Tyto alba) could detect changes in the spectral profile of multi-component auditory signals with stochastic envelope patterns. Signals consisted of one or five bands of noise (bandwidth 4, 16, or 64 Hz each; center frequencies 1.02, 1.43, 2.0, 2.8, 3.92 kHz). We determined increment thresholds for the 2 kHz component for three conditions: single-band condition (only the 2 kHz component), all five noise bands with the envelope fluctuations of the bands being either correlated or uncorrelated. Noise bandwidth had no significant effect on increment detection. Increment thresholds for the different conditions, however, differed significantly. Thresholds in correlated conditions were generally the lowest of all conditions, whereas, thresholds in uncorrelated conditions mostly resulted in the highest thresholds. This can be interpreted as evidence for comodulation masking release in barn owls. If the increment in the 2 kHz component is balanced by decrementing the four flanking bands in amplitude, increment detection thresholds are not affected. The data suggest that the barn owls used information from simultaneous spectral comparison across different frequency channels to detect spectral changes in multi-component noise signals rather than sequential comparison of overall stimulus levels.     

Role of corticofugal feedback in hearing

The auditory system consists of the ascending and descending (corticofugal) systems. The corticofugal system forms multiple feedback loops. Repetitive acoustic or auditory cortical electric stimulation activates the cortical neural net and the corticofugal system and evokes cortical plastic changes as well as subcortical plastic changes. These changes are short-term and are specific to the properties of the acoustic stimulus or electrically stimulated cortical neurons. These plastic changes are modulated by the neuromodulatory system. When the acoustic stimulus becomes behaviorally relevant to the animal through auditory fear conditioning or when the cortical electric stimulation is paired with an electric stimulation of the cholinergic basal forebrain, the cortical plastic changes become larger and long-term, whereas the subcortical changes stay short-term, although they also become larger. Acetylcholine plays an essential role in augmenting the plastic changes and in producing long-term cortical changes. The corticofugal system has multiple functions. One of the most important functions is the improvement and adjustment (reorganization) of subcortical auditory signal processing for cortical signal processing.     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Evoked cochlear potentials in the barn owl

Gross electrical responses to tone bursts were measured in adult barn owls, using a single-ended wire electrode placed onto the round window. Cochlear microphonic (CM) and compound action potential (CAP) responses were evaluated separately. Both potentials were physiologically vulnerable. Selective abolishment of neural responses at high frequencies confirmed that the CAP was of neural origin, while the CM remained unaffected. CAP latencies decreased with increasing stimulus frequency and CAP amplitudes were correlated with known variations in afferent fibre numbers from the different papillar regions. This suggests a local origin of the CAP along the tonotopic gradient within the basilar papilla. The audiograms derived from CAP and CM threshold responses both showed a broad frequency region of optimal sensitivity, very similar to behavioural and single-unit data, but shifted upward in absolute sensitivity. CAP thresholds rose above 8 kHz, while CM responses showed unchanged sensitivity up to 10 kHz.     

Commissural connections mediate inhibition for the computation of interaural level difference in the barn owl

Summary In the barn owl (Tyto alba), the posterior nucleus of the ventral lateral lemniscus (VLVp) is the first site of binaural convergence in the pathway that processes interaural level difference (ILD), an important sound-localization cue. The neurons of VLVp are sensitive to ILD because of an excitatory input from the contralateral ear and an inhibitory input from the ipsilateral ear. A previously described projection from the contralateral cochlear nucleus, can account for the excitation. The present study addresses the source of the inhibitory input.We demonstrate with standard axonal transport methods that the left and right VLVps are interconnected via fibers of the commissure of Probst. We further show that the anesthetization of one VLVp renders ineffective the inhibition that is normally evoked by stimulation of the ipsilateral ear. Thus, one cochlear nucleus (driven by the ipsilateral ear) appears to provide inhibition to the ipsilateral VLVp by exciting commissurally-projecting inhibitory neurons in the contralateral VLVp.Abbreviations ABL average binaural level - CP commissure of Probst - DNLL dorsal nucleus of the lateral lemniscus - IC inferior colliculus - ILD interaural level difference - IPc nucleus isthmi, pars parvocellularis - ITD interaural time difference - LSO lateral superior olive - MNTB medial nucleus of the trapezoid body - NA nucleus angularis - SL nucleus semilunaris - VLVa nucleus ventralis lemnisci lateralis, pars anterior - VLVp nucleus ventralis lemnisci lateralis, pars posterior     

An auditory fovea in the barn owl cochlea

The distribution of frequencies along the basilar papilla of the barn owl (Tyto alba) was studied by labelling small groups of primary auditory neurones of defined frequency response and tracing them to their peripheral innervation sites. The exact location of marked neurones was determined in cochlear wholemounts with the aid of a special surface preparation technique. The average basilar papilla length (in fixed, embedded specimens) was 10.74 mm.The resulting frequency map shows the basic vertebrate pattern with the lowest frequencies represented apically and increasingly higher frequencies mapped at progressively more basal locations. However, the length of basilar papilla devoted to different frequency ranges, i.e. the space per octave, varies dramatically in the barn owl. The lower frequencies (up to 2 kHz) show values between about 0.35 and 1 mm/octave, which are roughly equivalent to values reported for other birds. Above that, the space increases enormously, the highest octave (5–10 kHz) covering about 6 mm, or more than half of the length of the basilar papilla.Such an overrepresentation of a narrow, behaviourally very important frequency band is also seen in some bats, where it has been termed an acoustic or auditory fovea.Abbreviations CF characteristic frequency - HRP horseradish peroxidase - NA Nucleus angularis - NM Nucleus magnocellularis     

Progressive plasticity of auditory cortex during appetitive operant conditioning

In stimulus-response-outcome learning, different regions in the cortico-basal ganglia network are progressively involved according to the stage of learning. However, the involvement of sensory cortex remains ellusive even though massive cortical projections to the striatum imply its significant role in this learning. Here we show that the global tonotopic representation in the auditory cortex changed progressively depending on the stage of training in auditory operant conditioning. At the early stage, tone-responsive areas mainly in the core cortex expanded, while both the core and belt cortices shrank at the late stage as behavior became conditioned. Taken together with previous findings, this progressive global plasticity from the core to belt cortices suggests differentiated roles in these areas: the core cortex serves as a filter to better identify auditory objects for hierarchical computation within the belt cortex, while the belt stores auditory objects and affects decision making through direct projections to limbic system and higher association cortex. Thus, the progressive plasticity in the present study reflects a shift from identification to storage of a behaviorally relevant auditory object, which is potentially associated with a habitual behavior.     

Spatial and spectral dependence of the auditory periphery in the northern leopard frog

We investigated directionalities of eardrum vibration and auditory nerve response in anesthetized northern leopard frogs (Rana pipiens pipiens). Simultaneous measures of eardrum velocities and firing rates from 282 auditory nerve fibers were obtained in response to free-field sounds from eight directions in the horizontal plane. Sound pressure at the external surface of the ipsilateral eardrum was kept constant for each presentation direction (± 0.5 dB). Significant effects of sound direction on eardrum velocity were shown in 90% of the cases. Maximum or minimum eardrum velocity was observed more often when sounds were presented from the lateral and posterior fields, or from the anterior and contralateral fields, respectively. Firing rates of 38% of the fibers were significantly affected by sound direction and maximum or minimum firing rate was observed more frequently when sounds were delivered from the lateral fields, or from the anterior and contralateral fields, respectively. Directionality patterns of eardrum velocity and nerve firing also vary with sound frequency. Statistically significant correlation between eardrum velocity and nerve fiber firing rate was demonstrated in only 45% of the fibers, suggesting that sound transmission to the inner ear through extratympanic pathways plays a non-trivial role in the genesis of directionality of auditory nerve responses.Abbreviations CF characteristic frequency - SVL snout-vent length - TM tympanic membrane     

Prolonged maturation of cochlear function in the barn owl after hatching

Cochlear microphonics (CMs), which represent the electrical activity of hair cells, and compound action potentials (CAPs), which represent the activity of the auditory nerve, were recorded from the round window of the inner ear, in owlets aged between 5 and 97 days posthatching, i.e., from soon after hatching to beyond fledgling. At the earliest ages examined, animals showed very insensitive CM and virtually no CAP responses. Thus, hearing in barn owls develops entirely posthatching and the birds appear to be profoundly deaf well into the second week. Thresholds improved gradually after that and CMs reached their adult sensitivity at 5 weeks posthatching at all frequencies. Compound action potential responses appeared progressively later with increasing frequency. Adult neural sensitivity was achieved about 1 week later than for the CM responses at most frequencies, but took until 9–10 weeks posthatching at the highest frequencies (8–10 kHz). This indicates an apex-to-base maturation sequence of neural sensitivity within the cochlea, with a disproportionately long period to maturity for the most basal regions. Compound action potential amplitudes matured even later, at about 3 months posthatching, at all frequencies. This suggests a prolonged immaturity in the temporal synchrony of spiking in the auditory nerve.     

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. Accepted: 18 January 2000     

听觉电生理实时分析系统及其在大鼠下丘信息编码研究中的应用

基于TDT神经电生理软硬件平台和Matlab软件环境,开发了专用于听觉电生理研究的实时分析软件。通过对神经元胞外记录信号的在线处理和分析,可以在实验过程中得到刺激后放电活动时间直方图、平均发放率、首次发放潜伏期等定量分析结果,以及刺激参数变化时神经元发放率的变化曲线,如发放率-刺激强度曲线等。此分析软件被用于大鼠下丘神经元听觉信息编码的研究中,观察到下丘神经元对于纯音和噪声刺激不同的时间响应模式,以及神经元发放率和首次发放潜伏期对声音刺激强度的编码。     

Directionality of the pressure-difference receiver ears in the northern leopard frog, Rana pipiens pipiens

We studied the directional response of the coupled-eardrum system in the northern leopard frog, Rana pipiens pipiens. Eardrum behavior closely approximates a linear time-invariant system, with a highly correlated input–output relationship between the eardrum pressure difference and the eardrum velocity. Variations in the eardrum transfer function at frequencies below 800 Hz indicate the existence of an extratympanic sound transmission pathway which can interfere with eardrum motions. The eardrum velocity was shown to shift in phase as a function of sound incident angle, which was a direct result of the phase-shift of the eardrum pressure difference. We used two laser-Doppler vibrometers to measure the interaural vibration time difference (IVTD) and the interaural vibration amplitude difference (IVAD) between the motions of the two eardrums. The coupled-eardrum system enhanced the IVTD and IVAD by a factor of 3 and 3 dB, respectively, when compared to an isolated-eardrum system of the same size. Our findings are consistent with the time-delay sensitivity of other coupled-eardrum systems such as those found in crickets and flies.