Willem J.M. Epping

Stimulus dependent neural correlations in the auditory midbrain of the grassfrog (Rana temporaria L.)

Few-unit recordings were obtained using metal microelectrodes. Separation into single-unit spike trains was based on differences in spike amplitude and spike waveform. For that purpose a hardware microprocessor based spike waveform analyser was designed and built. Spikes are filtered by four matched filters and filter outputs at the moments of spike occurrence are read by a computer and used for off-line separation and spike waveform reconstruction. Thirthy-one double unit recordings were obtained and correlation between the separated spike trains was determined. After stimulus correction correlation remained in only 8 of the double unit records. It appeared that in most cases this neural correlation was stimulus dependent. Continuous noise stimulation resulted in the strongest neural correlation remaining after correction for stimulus coupling, stimulation with 48 ms duration tonepips presented once per second generally did not result in a significant neural correlation after the correction procedure for stimulus lock. The usefulness of the additive model for neural correlation and the correction procedure based thereupon is discussed.

Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. II. Stimulation with amplitude modulated sound.

The coding of fine-temporal structure of sound, especially of frequency of amplitude modulation, was investigated on the single-unit level in the auditory midbrain of the grassfrog. As stimuli sinusoidally amplitude modulated sound bursts and continuous sound with low-pass Gaussian noise amplitude modulation have been used. Both tonal and wideband noise carriers have been applied. The response to sinusoidally amplitude modulated sound bursts was studied in two aspects focussing on two types of possible codes: a rate code and a synchrony code. From the iso-intensity rate histogram five basic average response characteristics as function of modulation frequency have been observed: low-pass, band-pass, high-pass, bimodal and non-selective types. The synchronization capability, expressed in a synchronization index, was non-significant for 38% of the units and a low-pass function of modulation frequency for most of the other units. The stimulus-response relation to noise amplitude modulated sound was investigated by a non-linear system theoretical approach. On the basis of first- and second-order Wiener-Volterra kernels possible neural mechanisms accounting for temporal selectivity were obtained. About one quarter of the units had response characteristics that were invariant to changes in sound pressure level and spectral content of the carrier. These units may function as feature detectors of fine-temporal structure of sound. The spectro-temporal sensitivity range of the auditory midbrain of the grassfrog appeared not to be restricted to and showed no preference for the spectro-temporal characteristics of the ensemble of conspecific calls. Comparison of response characteristics to periodic click trains as studied in the companion paper (Epping and Eggermont, 1986) and sinusoidally amplitude modulated sound bursts revealed that the observed temporal sensitivity is due to a combination of sensitivities to sound periodicity and pulse duration. It was found that for most units the first-order kernels for Gaussian amplitude modulated stimuli and Poisson distributed click stimuli were alike. In contrast second-order kernels for the Gaussian amplitude modulated stimuli often represented only static non-linearities, while second-order kernels for Poisson distributed clicks (Epping and Eggermont, 1986) mostly revealed dynamic non-linearities.

Directional hearing in the grass frog ( Rana temporaria L.): I. Mechanical vibrations of tympanic membrane

The vibration characteristics (amplitude and phase as a function of frequency) of the tympanic membrane in the grass frog were measured using a laser-doppler velocity meter. It was tested to what extent the frogs acoustic system behaves as a pressure gradient receiver. This might clarify how the frog localizes sound. Using a closed sound system the membrane was stimulated at three different entrances: in front of the membrane, at the contralateral ear and from inside the mouth. A combination of these can describe the motion of the membrane under free field conditions. It is found that the sound entrance from inside the mouth will give almost identical vibration characteristics as stimulation in front of the membrane. This can yield a perfect gradient receiver mechanism, when the frog opens its mouth. It is doubted however whether the frog in nature needs to open its mouth for localization of sound. With mouth closed the effectiveness of the gradient receiver will be determined by the transmission characteristics of sound across the tissues of the mouth. The entrance of sound via the contralateral ear is only effective at frequencies between 800 and 1600 Hz. At those frequencies crosstalk between the membranes is however not more than -4 to -8 dB. This is subject to changes in the acoustic properties of the mouth cavity and can possibly be altered by the frog in free nature.

From Synchrony to Harmony: Ideas on the Function of Neural Assemblies and on the Interpretation of Neural Synchrony

Point of departure are experimental data acquired by simultaneous recording of the activity of a number (2–16) of individual neurons during presentation of a sensory stimulus. The area under investigation is the auditory midbrain (Torus semicircularis) of the immobilized grassfrog (Rana temporaria L.). The sensory stimuli are both artificial (noise, tones and clicks) and natural sounds (vocalizations and environmental sounds). The goal of investigation is an insight into the neural representation of the sensory environment.

Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. I. Stimulation with acoustic clicks

The coding of fine-temporal structure of sound, especially pulse repetition rate, was investigated on the single-unit level in the auditory midbrain of the grassfrog. As stimuli periodic click trains and Poisson distributed click ensembles have been used. The response to periodic click trains was studied in two aspects, focussing on two types of possible codes: a rate code and a synchrony code. From the iso-intensity rate histogram five basic average response rate characteristics as function of pulse repetition rate have been established: low-pass, band-pass, high-pass, bimodal and non-selective unit types. The synchronization capability, expressed in a synchronization index, was for a small majority of units non-significant and a low-pass function of pulse repetition rate for most of the other units. The rate code showed the largest diversity of response types and an enhanced selectivity to pulse repetition rate. The stimulus-response relation to Poisson distributed click ensembles was investigated by a non-linear system theoretical approach. On the basis of first- and second-order Poisson kernels possible neural mechanisms accounting for temporal selectivity were determined. A considerable fraction of units exhibited response characteristics that were invariant to changes in sound pressure level and average click rate. These units may function as feature detectors of fine-temporal structure of sound. The spectro-temporal sensitivity range of the auditory midbrain of the grassfrog appeared to be broad and not particularly tuned to the ensemble of conspecific cells.

Single-unit characteristics in the auditory midbrain of the immobilized grassfrog

The anuran auditory midbrain of the grassfrog (Rana temporaria L.) was studied by a combined spectro-temporal analysis of sound preceding neural events. From the spectro-temporal sensitivities (STS) estimates of best frequencies (BF) and latencies (LT) were derived. Several types of STSs were observed: monomodal excitatory STSs comprised about half of the cases. Bimodal excitatory STSs, i.e. STSs with two discrete excitation regions, were observed in about 25%. Trimodal and broadly tuned STSs comprised about 5%. The remaining 20% of the STSs were characterized by inhibitory phenomena such as pure inhibition, sideband inhibition and post-activation inhibition. The distribution of best frequencies matches the frequency spectrum of the animals vocalizations. A relative absence of monomodal units was noted in the mid frequency range. The distribution of latencies was bimodal over the range 7-108 ms. For each unit 6 functional parameters were determined; besides BF and LT these were: form of the STS (i.e. monomodality versus multimodality), spontaneous activity, binaural interaction, and firing mode (i.e. sustained versus transient) upon continuous noises stimulation. In addition, two structural parameters were considered: location in the torus and action potential waveform. Large correlations appeared between LT and action potential waveform, and between BF and binaural interaction type. Tonotopy was not found. A comparison was made between results from this study with a previous study on lightly anesthetized grassfrogs, using the same stimulus paradigms (D.J. Hermes et al. (1981): Hearing Res. 5, 147-178; D.J. Hermes et al. (1982): Hearing Res. 6, 103-126). Spontaneous activity, inhibitory phenomena and complex STSs were common using immobilization, whereas these have hardly been observed using anesthesia. Furthermore, interdependencies between the neural characteristics are substantially weaker for the immobilized preparation.

Sensitivity of neurons in the auditory midbrain of the grassfrog to temporal characteristics of sound. III. Stimulation with natural and synthetic mating calls

Using an ensemble of natural and synthetic mating calls we studied the single unit (N = 189) and small neuronal group (91 unit pairs) responsiveness in the auditory midbrain of the grassfrog. We compared this responsiveness to that obtained for toneburst and sine-modulated stimuli in order to reveal the presence of so-called mating call detectors. Under the set of stimuli used 5% of the single units appeared to respond selectively to the natural mating call. Simultaneously recorded units appeared to have in about half of the cases identical properties, in the other half even completely complementary properties were found. These properties are related to the organizational structure of the torus semicircularis. A mechanism of feature extraction based on near coincident firings in simultaneously recorded neurons is presented.

Selectivity for temporal characteristics of sound and interaural time difference of auditory midbrain neurons in the grassfrog: A system theoretical approach

The selectivity for temporal characteristics of sound and interaural time difference (ITD) was investigated in the torus semicircularis (TS) of the grassfrog. Stimuli were delivered by means of a closed sound system and consisted of binaurally presented Poisson distributed condensation clicks, and pseudo-random (RAN) or equidistant (EQU) click trains of which ITD was varied. With RAN and EQU trains, 86% of the TS units demonstrated a clear selectivity for ITD. Most commonly, these units had monotonically increasing ITD-rate functions. In general, units responding to Poisson clicks, responded also to RAN and EQU trains. One category of units which showed strong time-locking had comparable selectivities for ITD with both stimulus ensembles. A second category of units showed a combined selectivity for temporal structure and ITD. These units responded exclusively to EQU trains in a nonsynchronized way. From the responses obtained with the Poisson click ensemble so-called Poisson system kernels were determined, in analogy to the Wiener-Volterra functional expansion for nonlinear systems. The kernel analysis was performed up to second order. Contralateral (CL) first order kernels usually had positive or combinations of positive and negative regions, indicating that the contralateral ear exerted an excitatory or combined excitatory-inhibitory influence upon the neural response. Ipsilateral (IL), units were characterized by first order kernels which were not significantly different from zero, or kernels in which a single negative region was present. A large variety of CL second order kernels has been observed whereas rarely IL second order kernels were encountered. About 35% of the units possessed nonzero second order cross kernels, which indicates that CL and IL neural processes are interacting in a nonlinear way. Units demonstrating a pronounced selectivity for ITD, were generally characterized by positive CL combined with negative IL first order kernels. Findings suggested that, in the grassfrog, neural selectivity for ITD mainly is established by linear interaction of excitatory and inhibitory processes originating from the CL and IL ear, respectively. Units exhibiting strong time-locking to Poisson clicks and RAN and EQU trains had significantly shorter response latencies than moderately time-locking units. In the first category of units, a substantial higher number of nonzero first and second order kernels was observed. It was concluded that nonlinear response properties, as observed in TS units, most likely have to be ascribed to nonlinear characteristics of neural components located in the auditory nervous system peripheral to the torus semicircularis.

Relation of binaural interaction and spectro-temporal characteristics in the auditory midbrain of the grassfrog

The relation between binaural interaction type and spectro-temporal characteristics was studied for single units in the auditory midbrain of the grassfrog. Tonal and continuous wideband noise ensembles have been used as stimuli. Spectro-temporal sensitivities were determined for ipsi-, contra- and bilateral stimulus presentation by a closed sound system. Binaural interaction was classified in monaural EO (one ear excitatory), binaural EE (both ears excitatory) and EI (one ear excitatory, the other inhibitory) and purely inhibitory categories. Binaural interaction appeared to be rather invariant to alterations in stimulus intensity and type. A very clear correlation was observed between best frequency and binaural interaction type: EE units are predominantly of high best frequency, whereas EI units are predominantly of low best frequency. The correlation with latency was less significant: EE units tended to have somewhat shorter latencies that EI units. EO units take an intermediate position. Comparisons of ipsi-, contra- and bilateral spectro-temporal sensitivities, revealed differences in best frequency, latency and temporal discharge pattern. In some units a complex interplay of excitatory and inhibitory monaural influences was demonstrated. A number of units was recorded, which were characterized by multiple activation or suppression areas. The majority of these units exhibited frequency-dependent binaural interaction types. In some units it was noticed that binaural interaction type can be dependent on state of adaptation. A comparison of binaural interaction types of neighbouring units provided only weak evidence for a binaural organization in the anuran auditory midbrain, since simultaneously recorded pairs shared the same binaural interaction type only slightly more than expected by mere chance (chi 2-test, P less than 0.10).

Sensitivity for interaural time and intensity difference of auditory midbrain neurons in the grassfrog

The sensitivity for interaural time (ITD) and intensity (IID) difference was investigated for single units in the auditory midbrain of the grassfrog. A temporally structured stimulus was used which was presented by means of a closed sound system. At best frequency (BF) the majority of units was selective for ITD as indicated by an asymmetrically (73%) or symmetrically (7%) shaped ITD-rate histogram. About 20% appeared to be nonselective. Units with a symmetrical rate histogram had BFs well above 0.9 kHz, whereas for the other categories no relationship with BF was observed. Most units had a selectivity for ITD which was rather independent from frequency and absolute intensity level. In 62% of the units interaural time difference could be traded by interaural intensity difference. In most cases this so-called time-intensity trading could be explained by the intensity-latency characteristics of auditory nerve fibres. About 20% was sensitive to IID only and 5% to ITD only. A binaural model is proposed which is based on the intensity-rate and intensity-latency characteristics of auditory nerve fibres, the linear summation of excitatory and inhibitory post synaptic potentials in second order neurons, and spatiotemporal integration at the level of third order neurons. By variation of only a small number of parameters, namely strengths and time constants of the connectivities, the range of experimentally observed response patterns could be reproduced.