Joachim Ostwald

Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase

SummaryAn attempt was made to correlate electrophysiological and morphological characteristics of rat ventral cochlear nucleus neurons. Their axonal course and their soma morphology were investigated using the intra-axonal horseradish peroxidase method. Prior to labeling, neurons were characterized by recording their response patterns to acoustic stimulation with pure tones. Three types of cells were found: Category I (37 neurons) exhibited “primarylike” responses and a spontaneous firing rate below 10 spikes/s. Category II (21 neurons) showed “on” responses and little spontaneous activity. Category III (9 neurons) had “primarylike” responses like neurons in category I. However, the spontaneous activity rate of these neurons was significantly higher (mean: 95 spikes/s). Among the response categories, the morphological characteristics differed in some prominent aspects. Within each category, however, the morphological properties were rather similar. All neurons in category I were globular/bushy cells located in the area of the entrance of the cochlear nerve. The axon of each cell coursed along the ventral acoustic stria and consistently innervated the lateral superior olive ipsilaterally, and the nucleus of the trapezoid body and the nucleus of the lateral lemniscus contralaterally. Some neurons also projected to periolivary nuclei ipsilaterally and contralaterally. Neurons in category II were located in the posteroventral cochlear nucleus and were presumably multipolar/stellate cells. Their axons coursed via the intermediate acoustic stria and innervated mainly contralateral periolivary regions as well as the contralateral nucleus of the lateral lemniscus. Ipsilaterally, the lateral superior olive and the superior periolivary nucleus were innervated by some of the category II neurons. Somata types of neurons in category III could not be identified morphologically, but somata were located in caudal parts of the posteroventral cochlear nucleus that correspond to the octopus cell area. Their axons coursed via the intermediate acoustic stria and innervated periolivary regions and the contralateral nucleus of the lateral lemniscus. Thus, their axonal distribution differed only slightly from neurons in category II. These data confirm and extend previous findings regarding the efferent connections of ventral cochlear neurons. They emphasize the complexity of the axonal projection patterns of single cochlear nucleus cells. Since two types of response patterns and three types of axonal projection patterns have been observed, there remains an ambiguous relation between response pattern and axonal projection site. It is concluded that the response pattern to pure tone stimulation alone is not sufficient to describe physiological characteristics allowing for the establishment of structure-function relations. Only if one considers additional physiological properties like the spontaneous activity rate and the shape of tuning curves, does a correspondence between structure and function become apparent.

TEMPORAL CODING OF AMPLITUDE AND FREQUENCY MODULATION IN THE RAT AUDITORY CORTEX

The rat primary auditory cortex was explored for neuronal responses to pure tones and sinusoidally amplitude‐modulated (SAM) and frequency‐modulated (SFM) stimuli. Units showed phase‐locked responses to SAM stimulation (55%) and SFM stimulation (80%), with modulation frequencies up to 18 Hz. Tuning characteristics to the modulation frequency were mainly band‐pass with best modulation frequencies (BMFs) between 4 and 15 Hz. Units with synchronized activity to SFM stimulation showed three response types with respect to the direction of the frequency modulation: 52% were selective to the upward direction, 30% to the downward direction, and 18% had no preference. Triangular frequency modulations were used to test if units were tuned to specific modulation frequencies or to specific rates of frequency change. In the vast majority of units tested the response characteristics were strongly influenced by varying the modulation frequency, whereas varying the rate of frequency change had little effect in the stimulus range used. Units that showed phase‐locked responses to SAM and SFM stimulation had similar activity patterns in response to both types of stimuli. BMFs for SAM and SFM stimulation were significantly correlated. Intrinsic oscillations of up to 20 Hz could be seen in the spontaneous activity and after the stimuli independent of the stimulus type. Oscillation frequencies were significantly correlated with the BMFs of the respective units. The results are discussed in terms of a mechanism for periodicity detection based on a temporal code. This could be important for the recognition of complex acoustic signals.

Serotonin modulates auditory information processing in the cochlear nucleus of the rat

The effect of iontophoretic application of serotonin (5-HT) was studied in neurons of the cochlear nucleus in the rat. 5-HT inhibited the spontaneous activity in 71%, and the tone-evoked activity in 32% of the neurons. We also observed an excitatory effect, with a longer latency than that of the inhibition, in 40% of the neurons. In some neurons 5-HT had both inhibitory and excitatory effects. Neurons with different response types seem to have different sensitivities to 5-HT. As the effects of 5-HT were generally weaker than those of other putative neurotransmitters, it probably has only a small modulatory influence on auditory processing.

Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the Greater Horseshoe Bat

SummaryTonotopical organization and frequency representation in the auditory cortex of Greater Horseshoe Bats was studied using multi-unit recordings.The auditory responsive cortical area can be divided into a primary and a secondary region on the basis of response characteristics forming a core/belt structure.In the primary area units with best frequencies in the range of echolocation signals are strongly overrepresented (Figs. 6–8). There are two separate large areas concerned with the processing of the two components of the echolocation signals. In one area frequencies between the individual resting frequency and about 2 kHz above are represented, which normally occur in the constant frequency (CF) part of the echoes (CF-area), in a second one best frequencies between resting frequency and about 8 kHz below are found (FM-area).In the CF-area tonotopical organization differs from the usual mammalian scheme of dorso-ventral isofrequency slabs. Here isofrequency contours are arranged in a semicircular pattern.The representation of the cochlear partition (cochleotopic organization) was calculated. In the inferior colliculus and auditory cortex there is a disproportionate representation of the basilar membrane. This finding is in contradiction to the current opinion that frequency representation in the auditory system of Horseshoe Bats is only determined by the mechanical tuning properties of the basilar membrane.Response characteristics for single units were studied using pure tone stimuli. Most units showed transient responses. In 25% of units response characteristics depended on the combination of frequency and sound pressure level used.Frequency selectivity of units with best frequencies in the range of echolocation sounds is very high. Q-10dB values of up to 400 were found in a small frequency band just above resting frequency.

Adaptations for the Detection of Fluttering Insects by Echolocation in Horseshoe Bats

Comparative studies on echolocation in various species of bats reveal differences in the design of transmitters — i.e., the vocal systems producing different echolocation signals — as well as receivers — i.e., the auditory systems evaluating the echoes. Our hypothesis is that these differences reflect adaptations to the specific orientation tasks of each species.

The role of pinna movement for the localization of vertical and horizontal wire obstacles in the greater horseshoe bat, Rhinolopusferrumequinum

Six Rhinolophus ferrumequinum were trained to fly through an array of vertical or horizontal wires. Obstacle avoidance performance was measured as the percentage of flights in which the bats did not touch the wires (successful flights). Bats with normal mobile pinnae scored between 70% and 90% successful flights both with vertical and horizontal wires. After surgically immobilizing the pinnae by cutting motor nerves and ear muscles, avoidance performance with vertical wires (horizontal target localization) was unchanged but the percentage of successful flights with horizontal wires (vertical target localization) decreased significantly. This demonstrates the importance of pinna movements for target localization in the vertical plane and supports the hypothesis that scanning movements with pinnae are used by Rhinolophus ferrumequinum for determination of target angle.

Distribution of cochlear efferents and olivo-collicular neurons in the brainstem of rat and guinea pig

SummaryIn rat and guinea pig, cochlear efferents to the two ears were labeled simultaneously with different fluorescent tracers. It was found that in both species only few (1–3%) olivo-cochlear neurons were double-labeled and project to both cochleae. In most periolivary regions large olivocochlear neurons (OCN) projecting to the ipsilateral and contralateral side are intermingled and form a continuous cell column between the facial nucleus and lateral lemniscus. In a second series of experiments in rat, cochlear efferents and ascending olivo-collicular neurons were labeled. Olivo-cochlear and olivo-collicular neurons are intermingled in the lateral superior olive (LSO) and in the ventromedial periolivary region. No double-labeled neurons were found that project to the cochlea and the inferior colliculus.

Substance P and other putative transmitters modulate the activity of reticular pontine neurons: an electrophysiological and immunohistochemical study

In this study we investigated the effects of possible modulatory transmitters on acoustically responsive neurons of the caudal pontine reticular nucleus (PnC). From previous work in our laboratory it has been suggested that the acoustically responsive giant neurons of this nucleus are the sensorimotor interface mediating the acoustic startle response. Furthermore they are the site of some of the modulatory influence impinging on this response. Besides a possibly glutamatergic excitation from the amygdala a cholinergic input from the midbrain has been described which may use substance P as cotransmitter. Therefore we used electrophysiological and histochemical methods to study this possible modulatory influence in the caudal pontine reticular nucleus. In the first part of this study we recorded extracellularly from single units in the PnC in vivo and studied the effects of iontophoretically applied transmitters. Substance P elicited a long lasting excitation. This excitatory effect of SP was potentiated by acetyl-beta-methylcholine (AMCh, an acetylcholine agonist), whereas single application of AMCh showed no uniform response. Glutamate elicited a potent brief excitation, while application of GABA showed a potent brief inhibition of PnC neurons. In the second part of this study we employed immunoperoxidase staining for substance P, which revealed a fairly dense network of substance P-immunoreactive (SP-ir) fibers in the lateral and ventral aspects of the PnC. Combining retrograde tracing and immunocytochemistry for substance P, we demonstrated that the SP-ir axons in the PnC originate mainly in the laterodorsal tegmental nucleus. We therefore conclude that activation of the laterodorsal tegmental nucleus may facilitate the acoustic startle response by a long lasting excitation of neurons in the caudal pontine reticular nucleus.

Startle responses measured in muscles innervated by facial and trigeminal nerves show common modulation.

Electromyographic (EMG) potentials of several head muscles were recorded simultaneously in freely moving rats with chronically implanted electrodes. The startle responses of m. temporalis, m. levator auris, and m. levator labii superior were compared. All muscles showed a parallel decrease in latency and an increase in response elicitability and amplitude with an increase in stimulus intensity. A significant latency difference of about 1 ms existed between m. levator auris and m. temporalis. The shortest latency of the EMG response in m. levator auris was 5.5 ms (110 dB SPL). A common fluctuation in response amplitude and latency was found in simultaneous recordings of muscles innervated by the facial and trigeminal nerve, respectively. This shows a common modulatory input to the startle pathway to the cranial motor nuclei.

Comparative threshold studies of the acoustic pinna, jaw and startle reflex in the rat

Electromyograms of M. Levator auris and M. Temporalis and movement produced by whole body startle were recorded simultaneously in awake, freely moving rats. Thresholds were 78 db SPL for the L. auris, 80 dB SPL for the ballistic and 81 dB SPL for the Temporalis. The rank ordering of the three thresholds was extremely strict, 188 suprathreshold M. L. auris responses could be observed without M. Temporalis responses, but only once was a M. Temporalis response observed without a M. L. auris response. Thresholds as well as amplitudes and latencies measured by the different methods show correlated fluctuations. While the rise in amplitude which accompanies increasing stimulus intensity is similar in the three measures, the latency decrease is not. The latency difference between M. Temporalis EMG and M. L. auris EMG is intensity dependent, increasing from 0 msec at 78 dB SPL to 1.1 msec at 115 dB SPL, with a faster response for the M. L. auris.