Central representation of spatial and temporal surface wave parameters in the African clawed frog.

Xenopus laevis employs mechano-sensory lateral lines to, for instance, capture arthropods on the surface of turbid waters with poor visibility based on incoming wave signals. To characterise central representations of surface waves emitted from different locations, responses to several wave parameters were extracellularly recorded across brainstem, midbrain and thalamic areas. Overall, 339 of 411 statistically analysed responses showed significantly altered spike rates during the presentation of surface waves. Of these units, 45.1% were obtained in the torus semicircularis including its laminar subnucleus (23.3%) that is known to process auditory cues. Wave parameters contributing to central object representations were indicated by response rates that systematically varied with amplitude (76.3% of 160 tested units), frequency (74.4% of 270 tested units), source angle (93.7% of 79 tested units), or source distance (63.8% of 218 tested units). Map-like parameter representations were rather diffuse, yet an increased fraction of units tuned to frontal source angles was observed at deeper tissue layers (>180 µm), and an increased fraction of best neuronal responses to low wave frequencies (≤25 Hz) at rostral midbrain sections. Responses to wave frequencies remained largely robust across tested unit samples independent of source angles, and distances (N = 62). In comparison, spatial response characteristics seemed fragile across different wave frequencies in 68.3% of 41 recordings.

Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition.

The dominant cue for localization of low-frequency sounds are microsecond differences in the time-of-arrival of sounds at the two ears [interaural time difference (ITD)]. In mammals, ITD sensitivity is established in the medial superior olive (MSO) by coincidence detection of excitatory inputs from both ears. Hence the relative delay of the binaural inputs is crucial for adjusting ITD sensitivity in MSO cells. How these delays are constructed is, however, still unknown. Specifically, the question of whether inhibitory inputs are involved in timing the net excitation in MSO cells, and if so how, is controversial. These inhibitory inputs derive from the nuclei of the trapezoid body, which have physiological and structural specializations for high-fidelity temporal transmission, raising the possibility that well timed inhibition is involved in tuning ITD sensitivity. Here, we present physiological and pharmacological data from in vivo extracellular MSO recordings in anesthetized gerbils. Reversible blockade of synaptic inhibition by iontophoretic application of the glycine antagonist strychnine increased firing rates and significantly shifted ITD sensitivity of MSO neurons. This indicates that glycinergic inhibition plays a major role in tuning the delays of binaural excitation. We also tonically applied glycine, which lowered firing rates but also shifted ITD sensitivity in a way analogous to strychnine. Hence tonic glycine application experimentally decoupled the effect of inhibition from the timing of its inputs. We conclude that, for proper ITD processing, not only is inhibition necessary, but it must also be precisely timed.

Lateral line units in the amphibian brain could integrate wave curvatures.

Aquatic predators like Xenopus laevis exploit mechano-sensory lateral lines to localise prey on the water surface by its wave emissions. In terms of distance, hypothetically, the source of a concentric wave could be centrally represented based on wave curvatures: for Xenopus, we present a first sample of 98 extracellularly recorded brainstem and midbrain responses to waves with curvatures ranging from 22.2-11.1 m(-1). At the frog, concurrently, wave amplitudes and their spectral composition were kept stable. Notably, 61% of 98 units displayed curvature-dependent spike rates, suggesting that wave curvatures could support an extraction of source distances in the amphibian brain.

Neural responses to water surface waves in the midbrain of the aquatic predator Xenopus laevis laevis.

Many aquatic vertebrates use mechano-sensory lateral lines to decipher water movements. The peripheral and central organization of the lateral line system has much in common with the auditory system. Therefore, it was hypothesized that the information processing of both systems could be related. Analogous to acoustic objects, for instance, object representations along the central lateral line pathway must be generated from patterns of particle motion across peripheral receivers. Thus, the lateral line offers insight into key features of neural computation beyond a specific sensory system. Here, central processing of water surface waves was described in the African clawed frog which depends on wave signals for prey detection, recognition and localization. Neural responses to surface wave stimuli were recorded in the brainstem and midbrain of Xenopus. A total of 109 units displayed either excitatory or inhibitory responses to surface waves. The response pattern distribution differed significantly across the optic tectum and torus semicircularis magnocellularis (chi-square test, P < 0.05). Stimulus frequencies from 10 to 40 Hz were represented equally across lateral line nuclei but best frequencies were systematically distributed along the rostrocaudal axis of the midbrain (chi-square test, P < 0.05). Forty-one percent of 102 widely distributed units phase locked significantly to stimulus frequencies (Rayleigh test, P < 0.05; vector strength > 0.3) and 41% of 39 tested units featured non-monotone rate-level functions. These neurones were registered mainly in the dorsal tectum and magnocellular torus semicircularis (chi-square test, P < 0.05). Across all tested nuclei, 16 of 17 discreetly distributed units showed a directional response to spatial stimulation. The results suggest midbrain subdivisions with respect to processing of stimulus timing, frequency and amplitude.

Neural responses to free field and virtual acoustic stimulation in the inferior colliculus of the guinea pig.

Virtual auditory space (VAS) stimuli based on outer ear transfer functions became increasingly important in spatial hearing research. However, few studies have investigated the match between responses of auditory neurons to VAS and free-field (FF) stimulation. This study validates acoustic spatial receptive fields (SRFs) of 183 individual midbrain units using both VAS and FF stimuli. The first-spike latency, which varied systematically across SRFs, was 14.9 +/- 8.3 (SD) ms in FF, and 15.1 +/- 8.3 ms in VAS. Spike-count-based SRFs measured 0-20 dB above the neural threshold covered on average 44.5 +/- 18.0% of the recorded sphere in FF and 45.5 +/- 18.7% in VAS. The average deviation of the centroid position of SRFs using FF and VAS stimuli was 7.4 degrees azimuth and 3.3 degrees elevation. The average spike rate remained unchanged. The SRF overlap recorded using FF and VAS stimuli (mean: 71.3 +/- 12.6%) or repeated FF stimuli (70.2 +/- 14.2%) was high and strongly correlated (r = 0.96; P < 0.05). The SRF match observed with FF and VAS stimuli was not significantly altered over a range of stimulus levels (paired t-test P = 0.51; n = 6). Randomized VAS barely affected SRF sizes, centroids, or maximum spike count but decreased the average minimum response to 59% compared with sequential stimulation (paired t-test; P = 0.05; n = 26). SRF recordings in VAS excluding the acoustic distortions of the recording equipment differed from those in VAS incorporating the equipment (paired t-test P = 0.01; n = 5). In conclusion, neurophysiological recordings demonstrate that individualized VAS stimuli provided a good simulation of a FF environment.

Auditory response properties in the superior paraolivary nucleus of the gerbil.

The ascending auditory pathway is characterized by parallel processing. At the brain stem level, several structures are involved that are known to serve different well-defined functions. However, the function of one prominent brain stem nucleus, the rodent superior paraolivary nucleus (SPN) and its putative homologue in other mammals, the dorsomedial periolivary nucleus, is unknown. Based on extracellular recordings from anesthetized gerbils, we tested the role of the SPN in sound localization and temporal processing. First, the existence of binaural inputs indicates that the SPN might be involved in sound localization. Although almost half of the neurons exhibited binaural interactions (most of them excited from both sides), effects of interaural time and intensity differences (ITD; IID) were weak and ambiguous. Thus a straightforward function of SPN in sound localization appears to be implausible. Second, inputs from octopus and multipolar/stellate cells of the cochlear nucleus and from principal cells of the medial nucleus of the trapezoid body could relate to precise temporal processing in the SPN. Based on discharge types, two subpopulations of SPN cells were observed: about 60% of the neurons responded to pure tones with sustained discharges, with irregular spike patterns and no phase-locking. Only four neurons showed a regular spike pattern ("chopping"). About 40% of the neurons responded with phasic ON or OFF discharges. Average first spike latency observed in neurons with sustained discharges was significantly shorter than that of ON responders, but had a considerably higher trial-to-trial variation ("jitter"). A subpopulation of ON responders showed a jitter of less than +/-0.1 ms. Most neurons (66%) responded to sinusoidally amplitude-modulated sounds (SAM) with an ongoing response, phase-locked to the stimulus envelope. Again, ON responders showed a significantly higher temporal precision in the phase-locked discharge compared with the sustained responders. High variability was observed among spike-rate-based modulation transfer functions. Histologically, a massive concentration of cytochemical markers for glycinergic input to SPN cells was demonstrated. Application of glycine or its blockade revealed profound effects of glycinergic inhibition on the auditory responses of SPN neurons. The existence of at least two subpopulations of neurons is in line with different subsets of SPN cells that can be distinguished morphologically. One temporally less precise population might modulate the processing of its target structures by providing a rather diffuse inhibition. In contrast, precise ON responders might provide a short, initial inhibitory pulse to its targets.

Precise inhibition is essential for microsecond interaural time difference coding.

Microsecond differences in the arrival time of a sound at the two ears (interaural time differences, ITDs) are the main cue for localizing low-frequency sounds in space. Traditionally, ITDs are thought to be encoded by an array of coincidence-detector neurons, receiving excitatory inputs from the two ears via axons of variable length ('delay lines'), to create a topographic map of azimuthal auditory space. Compelling evidence for the existence of such a map in the mammalian lTD detector, the medial superior olive (MSO), however, is lacking. Equally puzzling is the role of a--temporally very precise glycine--mediated inhibitory input to MSO neurons. Using in vivo recordings from the MSO of the Mongolian gerbil, we found the responses of ITD-sensitive neurons to be inconsistent with the idea of a topographic map of auditory space. Moreover, local application of glycine and its antagonist strychnine by iontophoresis (through glass pipette electrodes, by means of an electric current) revealed that precisely timed glycine-controlled inhibition is a critical part of the mechanism by which the physiologically relevant range of ITDs is encoded in the MSO. A computer model, simulating the response of a coincidence-detector neuron with bilateral excitatory inputs and a temporally precise contralateral inhibitory input, supports this conclusion.