Effects of running water on brainstem lateral line responses in trout, Oncorhynchus mykiss, to sinusoidal wave stimuli.

We investigated how single units in the medial octavolateralis nucleus of the rainbow trout, Oncorhynchus mykiss, respond to a 50-Hz vibrating sphere in still and running water. Four types of units were distinguished. Type MI units ( N=16) were flow-sensitive; their ongoing discharge rates either increased or decreased in running water, and as a consequence, responses of these units to the vibrating sphere were masked if the fish was exposed to water flow. Type MII units ( N=7) were not flow-sensitive; their ongoing discharge rates were comparable in still and running water, and thus their responses to the vibrating sphere were not masked. Type MIII units ( N=7) were also not flow-sensitive; nevertheless, their responses to the vibrating sphere were masked in running water. Type MIV units ( N=14) were flow-sensitive, but their responses to the vibrating sphere were not masked. Our data confirm previous findings in the goldfish, Carassius auratus, indicating that the organization of the peripheral lateral line is reflected to a large degree in the medial octavolateralis nucleus. We compare data from goldfish and trout and discuss differences with respect to lateral line morphology, lifestyle and habitat of these species.

Brainstem lateral line responses to sinusoidal wave stimuli in the goldfish, Carassius auratus.

Extracellular recordings were made from single lateral line units in the medial octavolateralis nucleus in the brainstem of goldfish, Carassius auratus. Units were defined as receiving lateral line input if they responded to the water motions generated by a stationary, sinusoidally oscillating sphere and/or a moving sphere but not to airborne sound and vibrations. Units which responded to airborne sound or vibrations were assumed to receive input from the inner ear and were not further investigated. Responses of lateral line units were quantified in terms of the number of evoked spikes and the degree of phase-locking to a 50 Hz vibrating sphere presented at various stationary locations along the side of the fish. Receptive fields were characterized based on spike rate, degree of phase-locking and average phase angle as a function of sphere location. Four groups of units were distinguished: 1, units with receptive fields comparable to those of primary afferents; 2, units with receptive fields which consisted of one excitatory and one inhibitory area; 3, units with receptive fields which consisted of more than two excitatory and/or inhibitory areas; 4, units with receptive fields which consisted of a single excitatory or a single inhibitory area. The receptive fields of most units were characterized by adjacent excitatory and inhibitory areas. This organization is reminiscent of excitatory-inhibitory receptive field organizations in other vertebrate sensory systems.

The puzzle of hydrodynamic information processing: how are complex water motions analyzed by the lateral line?

We studied the discharges of neurons in the ascending lateral line pathway in response to the complex water motions generated by a moving object. The wave stimulus generated by the object was monitored with a hot-wire anemometer and with a custom-built particle imaging system. Responses of central lateral line neurons differ from those of primary afferent fibers in aspects like temporal discharge patterns and directional sensitivity. The data are consistent with the hypothesis that central lateral line neurons integrate input from many afferents innervating neuromasts distributed across large portions of the body surface.

Transformation of peripheral inputs by the first-order lateral line brainstem nucleus.

Extracellular recording techniques were used to record the responses of medial nucleus cells and posterior lateral line nerve fibers in mottled sculpin, Cottus bairdi, and goldfish, Carassius auratus, to a 50-Hz dipole source (vibrating sphere). Responses were characterized in terms of (1) receptive fields that relate responsiveness (spike rate and phase-locking) to the location of the source along the length of the fish, (2) input-output functions that relate responsiveness to vibration amplitude for a fixed source location, and (3) peri-stimulus time histograms that relate responsiveness to time during a sustained period of vibration. Relative to posterior lateral line nerve fibers, medial nucleus cells in both species were similar in showing (1) lower spontaneous and evoked rates of spike activity, (2) greater degrees of adaptation, (3) greater heterogeneity in all response characteristics, and (4) evidence for inhibitory/excitatory interactions. Whereas receptive fields of nerve fibers in both species faithfully reflect both pressure gradient amplitudes (with rate changes) and directions (with phase-angle changes) in the stimulus field, receptive fields of medial nucleus were more difficult to relate to the stimulus field, Some, but not all, receptive fields could be modeled with excitatory center/inhibitory surround and inhibitory center/excitatory surround organizations.

Sensitivity of central units in the goldfish, Carassius auratus, to transient hydrodynamic stimuli.

This study describes the discharges of central units in the medulla of the goldfish, Carassius auratus, to hydrodynamic stimuli received by the lateral line. We stimulated the animal with a small object moving in the water and recorded activity of 85 medullary lateral line units in response to different motion directions and to various object distances, velocities, accelerations and sizes. All but one unit increased discharge rate when the moving object passed the fish laterally. Five response types were distinguished based on temporal patterns of unit responses. Ten units were recorded which encoded motion direction by different temporal discharge patterns. In general, discharge rates decreased when object distance was increased and when object speed was decreased. When object size was decreased, discharge rates decreased systematically in one group of units, but they were comparable for all but the smallest object tested in a second group of units. Units responded about equally well whether an object was moved at a constant velocity or was accelerated when it passed the fish. The data indicate that medullary lateral line units in the goldfish can encode motion direction but are not tuned to other aspects of an object moving in the water. The functional properties of units in the medulla of goldfish are similar to those reported for medullary units in the catfish Ancistrus sp., suggesting that the central mechanisms for processing complex hydrodynamic stimuli may be quite similar in fish species that occupy habitats with different hydrodynamic conditions.

Site of auditory plasticity in the brain stem (VLVp) of the owl revealed by early monaural occlusion.

1. The optic tectum of the barn owl contains a physiological map of interaural level difference (ILD) that underlies, in part, its map of auditory space. Monaural occlusion shifts the range of ILDs experienced by an animal and alters the correspondence of ILDs with source locations. Chronic monaural occlusion during development induces an adaptive shift in the tectal ILD map that compensates for the effects of the earplug. The data presented in this study indicate that one site of plasticity underlying this adaptive adjustment is in the posterior division of the ventral nucleus of the lateral lemniscus (VLVp), the first site of ILD comparison in the auditory pathway. 2. Single and multiple unit sites were recorded in the optic tecta and VLVps of ketamine-anesthetized owls. The owls were raised from 4 wk of age with one ear occluded with an earplug. Auditory testing, using digitally synthesized dichotic stimuli, was carried out 8-16 wk later with the earplug removed. The adaptive adjustment in ILD coding in each bird was quantified as the shift from normal ILD tuning measured in the optic tectum. Evidence of adaptive adjustment in the VLVp was based on statistical differences between the VLVp's ipsilateral and contralateral to the occluded ear in the sensitivity of units to excitatory-ear and inhibitory-ear stimulation. 3. The balance of excitatory to inhibitory influences on VLVp units was shifted in the adaptive direction in six out of eight owls. In three of these owls, adaptive differences in inhibition, but not in excitation, were found. For this group of owls, the patterns of response properties across the two VLVps can only be accounted for by plasticity in the VLVp. For the other three owls, the possibility that the difference between the two VLVps resulted from damage to one of the VLVps could not be eliminated, and for one of these, plasticity at a more peripheral site (in the cochlea or cochlear nucleus) could also explain the data. In the remaining two owls, there was no evidence of adaptive adjustment in the VLVp despite large adaptive adjustments in the optic tectum. 4. The adjustment of ILD coding in the VLVp was always substantially smaller than expected based on the adjustment of ILD tuning in the optic tectum measured in the same animals. This indicates the involvement of at least one additional site of adaptive plasticity in the auditory pathway above the level of the VLVp.(ABSTRACT TRUNCATED AT 400 WORDS)

Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl's auditory system.

In the avian auditory system, the posterior division of the ventral nucleus of the lateral lemniscus (VLVp) is the first site where the levels of sound arriving at the two ears are compared. VLVp units are excited by sound at the contralateral ear and are inhibited by sound at the ipsilateral ear, and, as a result, are sensitive to interaural level differences (ILD). In this study, we investigate the functional properties of VLVp units and describe the topography of ILD sensitivity along the dorsoventral dimension of this nucleus. The responses of VLVp units were tested with monaural and binaural noise delivered through earphones. Excitatory and inhibitory responsiveness was quantified using several measures that assessed the effect of contra-ear stimulation and the effect of ipsi-ear stimulation on the contra-ear response. On the basis of these measures, we characterize the map of ILD sensitivity in the VLVp. The temporal pattern of unit responses were also analyzed. The discharges of VLVp units were regular and time-locked to the onset of a stimulus, a pattern of discharge reminiscent of the 'chopper pattern' observed in the lateral superior olive (LSO) of mammals. The temporal discharge patterns of a single VLVp neuron often distinguished between equivalent ILDs, resulting from different combinations of contra- and ipsi-ear levels, that were not distinguished by spike count alone. However, the temporal response pattern did not distinguish between all such combinations of contra- and ipsi-ear levels. The additional information was encoded by the pattern of activity across the entire population of VLVp neurons. This study describes similarities in the functional properties of VLVp and LSO units that suggest similar physiological mechanisms in avians and mammals for encoding similar acoustic information.

Early monaural occlusion alters the neural map of interaural level differences in the inferior colliculus of the barn owl.

Monaural occlusion during early life causes adaptive changes in the tuning of units in the owl's optic tectum to interaural level differences (ILD) that tend to align the auditory with the visual map of space. We investigated whether these changes could be due to experience-dependent plasticity occurring in the auditory pathway prior to the optic tectum. Units were recorded in the external nucleus of the inferior colliculus (ICx), which is a major source of auditory input to the optic tectum. The tuning of ICx units to ILD was measured in normal barn owls and in barn owls raised with one ear occluded. ILD tuning at each recording site was measured with dichotic noise bursts, presented at a constant average binaural level, 20 dB above threshold. The best ILD at each site was defined as the midpoint of the range of ILD values which elicited more than 50% of the maximum response. A physiological map of ILD was found in the ICx of normal owls: best ILDs changed systematically from right-ear-greater to left-ear-greater as the electrode progressed from dorsal to ventral. Best ILDs ranged from 13 dB right-ear-greater to 15 dB left-ear-greater and progressed at an average rate of 12 dB/mm. The representations of ILD were similar on both sides of the brain. In the ICx of owls raised with one ear occluded, the map of ILD was shifted in the adaptive direction: ILD tuning was shifted towards values favoring the non-occluded ear (the direction that would restore a normal space map). The average magnitude of the shift was on the order of 8-10 dB in each of 4 owls. In one owl, the mean shift in ILD tuning was almost identical on both sides of the brain. In another owl, the mean shift was much larger on the side ipsilateral to the occlusion than on the contralateral side. In both cases, the mean shifts measured in each ICx were comparable to the mean shifts measured in the optic tectum on the same sides of the brain. Thus, the adjustments in ILD tuning that have been observed in the optic tectum in response to monaural occlusion are almost entirely due to adaptive mechanisms that operate at or before the level of the ICx.

Discrimination of two-wavefront echoes by the big brown bat, Eptesicus fuscus: behavioral experiments and receiver simulations.

1. Echolocating bats (Eptesicus fuscus) were trained to discriminate between simulated targets consisting of one or two echo-wavefronts with internal time delays of up to 100 microseconds. Spectral and temporal properties and total signal energy of the targets were evaluated and predictions for performances of bats derived from receiver models were compared with measured performances. 2. Eptesicus fuscus was able to discriminate a one-wavefront target from two-wavefront targets with distinct internal time delays (12 microseconds, 32-40 microseconds and 52-100 microseconds). Performance was not affected by changes in total signal energy. Bats also successfully discriminated between two-wavefront targets with different internal time delays. 3. Performance predicted from differences in total energy between targets did not match the measured performance, indicating that bats did not rely on total echo energy. This finding is also supported by the behavioral data. Performance predicted from spectral and temporal receiver models both matched the measured performance and, therefore, neither one of these models can be favored over the other. 4. The behavioral data suggest that Eptesicus fuscus did not transform echo information into estimates of target range separation and, therefore, did not perceive the two wavefronts of each simulated two-wavefront echo as two separate targets.

Adaptive adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum.

Bimodal units in the barn owl's optic tectum are tuned to the location of auditory and visual stimuli, and are systematically organized according to their spatial tuning to form mutually aligned maps of auditory and visual space. Map alignment results from the fact that, normally, units are tuned to the values of interaural level difference (ILD) and interaural time difference (ITD) produced by a sound source at the location of their visual receptive fields (VRFs). Monaural occlusion alters the correspondence of ILD and ITD values with locations in space. We investigated the effect that raising owls with a chronic monaural occlusion has on the tuning of tectal units to ILD and ITD. Owls were monaurally occluded beginning at 1 month of age. The effects of monaural occlusion were assessed 2-4 months later by comparing the ILD and ITD tuning of units in monaurally occluded owls with the ILD and ITD tuning of units with equivalent VRFs in normal owls. ILD and ITD tuning was shifted substantially and in the direction of the unoccluded ear (the adaptive direction) in owls raised with a monaural occlusion. In most tecta, the mapped representations of ILD and ITD were shifted systematically. In addition, in some tecta, monaural occlusion induced a change in the topography of the ILD map such that ILD tuning remained essentially constant at values near 0 dB over abnormally large portions of the tectum. Across all recording sites, the average shift in ILD tuning was 9 dB (n = 396) and the average shift in ITD tuning was 40 microseconds (n = 414). In four of five animals, the magnitude of the effect was not equivalent on the two sides of the brain, the adjustments being significantly larger and more systematic on the side ipsilateral to the occlusion. Such differences in the altered ILD and ITD maps on the two sides of the brain in individual animals indicate that, although a component of the adaptive adjustment might be due to regulation of the gain and phase response of the monaural signals early in the auditory pathway, a major component of the adjustment must occur at or beyond the level where the encoding of ILDs and ITDs for left and right space separates.

Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum.

Neurons in the developing optic tectum adjust their tuning to auditory localization cues in response to chronic monaural occlusion so that auditory spatial fields align with visual receptive fields (VRFs). We tested whether this adaptive adjustment of auditory tuning requires visual instruction. Both eyelids were sutured closed at the same time that one ear was occluded in two barn owls that were 1 month old. After 70 and 100 d, respectively, the tuning of units to interaural level difference (ILD) and to interaural time difference (ITD) was measured. These data were compared with equivalent data from 15 normal owls. Unit tuning to ITD was shifted from normal in both of the monaurally occluded owls. In one owl, ILD tuning was also clearly shifted. In the other owl, the map of ILD was flipped upside down and adaptive adjustments in ILD tuning could not be assessed. Instead, adjustments in ILD tuning were observed following removal of the earplug with the eyelids kept closed. Unit tuning was monitored at several sites in the tectum for 1 month after earplug removal using chronically implanted electrodes. Then, ILD tuning was resampled across the entire tectum. Both measures indicated shifts in ILD tuning in response to removal of the earplug in the second blind owl. In both animals, the magnitude of the shifts in ILD tuning and ITD tuning was smaller than has been observed previously in monaurally occluded but sighted owls. The results demonstrate that the brain can make adaptive adjustments in ILD and ITD tuning in response to early monaural occlusion even without the guiding influence of vision.

Range resolution and the possible use of spectral information in the echolocating bat, Eptesicus fuscus.

Individuals of the echolocating bat Eptesicus fuscus were trained to discriminate simulated two-wave-front targets with internal time delays of 0 to 100 microns between the wave fronts from a one-wave-front target. The ability of bats to discriminate between such targets can be referred to as range resolution. In Eptesicus fuscus, this ability is limited to distinct internal time delays (12, 32-40, and 52-100 microns) between the two wave fronts of a double-wave-front target. Analysis of the simulated two-wave-front echoes reveals periodic frequency minima in the spectrum. Position and separation of these spectral minima depend on the time delay between the two wave fronts. The occurrence of spectral minima within the frequency range of the first harmonic in the echo of the bats' echolocation call correlates to the bats' ability to discriminate a one-wave-front echo from two-wave-front echoes, suggesting that Eptesicus fuscus uses spectral differences within the first harmonic in echoes for range resolution.