Peter Schlegel

Auditory physiological properties of the neurones in the inferior colliculus of the big brown bat,Eptesicus fuscus

Summary1.Electrophysiological properties of single units in the inferior colliculi of 9 big brown bats,Eptesicus fuscus, were studied by recording the responses of single units to pure tone pulses and frequency-modulated signals. Evoked potentials were also measured from 5 locations.2.Single units are tonotopically organized with low frequency units located dorsally, high frequency units ventrally and intermediate frequency units interposed between them.3.Response patterns of 230 units could be classified into six types but most units fired either tonically or phasically.4.The peak latency of the evoked potential is betwen 3.5 and 4.0 ms. Those of the 188 on-responding units are mainly between 5.0 and 12.5 ms.5.Threshold curves of the evoked potentials are broadly tuned to frequencies from 10 to 90 kHz. Those of single units are either broad, narrow or closed (upper threshold). The Q10−dB values range between 1.3 (BF = 31.4 kHz) and 39.5 (BF = 79 kHz) but the majority are below 24. Threshold curves of 4 on-off responders and 3 inhibitory units were also measured.6.The impulse-count functions of 109 units were either monotonic or non-monotonic. Among the 89 non-monotonic units, 17 had upper thresholds so that they stopped discharging action potentials when the stimulus became very intense (Fig. 10C). A series of the impulse-count function of 29 units to pure tone pulses and different FM stimuli were also measured.7.Minimum thresholds of 112 units to pure tone pulses and FM stimuli with different rates were compared. Most units had equal thresholds or within ±5 dB difference in thresholds to both pure tone pulses and FM stimuli. However, 15 units exclusively responded only to pure tone pulses.8.Responses of 35 units to different stimulus duration were studied. The number of impulses of single units either monotonically or non-monotonically increased with stimulus duration or maintained a rather constant level regardless of stimulus duration. Response patterns of some units changed drastically with stimulus duration.9.Responses of 33 units to different stimulus repetition rate were studied. The number of impulses of 26 units reached to the maximum value at a specific stimulus repetition rate. Those of the remaining 7 units either reached to the maximum over a broad range or maintained a rather constant level regardless of the repetition rate of a stimulus.

Comparative auditory neurophysiology of the inferior colliculus of two molossid bats,molossus ater andmolossus molossus

Summary1.Recordings were made from single inferior colliculus neurons of two closely related bat species,Molossus ater andMolossus molossus, both emitting short CF-FM echolocation calls which differ only in frequency range. Employing pure tone stimuli, minimum thresholds, tuning curves, response patterns and spike count functions were measured and compared between the two species.2.The audiograms (evoked potential measurements and distribution of single neuron thresholds) of both species are rather broadly tuned, but maximum auditory sensitivity is reached at different frequency ranges according to the different spectral content of the orientation calls.3.Single unit data concerning tuning curves, Q10dB-values, response patterns and spike count functions are very similar in the samples obtained from the two molossid species and closely resemble data from bats using FM-orientation calls.4.The inferior colliculus of molossids is tonotopically organized. Asymmetrical and symmetrical tuning curves were found. Q10dB-values rarely exceeded 20, and so are values known as characteristic for other mammals. The dominant response pattern class is the “phasic-on” type with no or low spontaneous activity. Spike count functions of the non-monotonic type prevail.5.Data are compared with results from “long CF-FM-bats”, revealing striking species differences in frequency selectivity of single neurons and organization of the ascending auditory pathway. This suggests different strategies in information processing which are discussed as adaptations to the species specific orientation calls.

Die Schwingungen der Antenne und ihre Bedeutung für die Flugsteuerung bei Calliphora erythrocephala

Summary1.Antennal movements of low frequency (10–20 c/sec, amplitude ≈+2.5°) are performed actively in the scape-pedicel joint during flight.2.Irregularities in the air currents from the wind tunnel cause smaller passive antennal movements of low frequency.3.Passive vibrations of the arista and the funicle (“antennal vibrations”) are superimposed on the active antennal movements. They form the mechanical stimulus component for the organ of Johnston, the aerodynamic sense organ of the pedicel. These vibrations are generated by the flight-tone and therefore they are similar in form and frequency to the thoracic vibrations.4.The resonance frequency of the antennal vibrations, when the pedicelfunicle joint is in the resting position, is 280 c/sec (♀♀) and 350 c/sec (♂♂) (Abb. 4). These values are much higher than the wing-stroke frequency (140 to 180 c/sec). As the speed of the air current is increased the deflexion of the pedicel-funicle joint increases and the resonance frequency rises. At the same time the amplitude of the antennal vibration decreases within the range of physiological frequencies (Abb. 6, 7).5.The organ of Johnston is most sensitive within the range of the wing-stroke frequency (Abb. 11–13). This maximal response is not caused by the mechanical resonance which occurs at much higher frequencies. It must therefore depend on properties of the stimulus transmitting structures or on the sense cells themselves. These properties can be distinguished from the mechanical resonance as some kind of “physiological resonance”.6.The action potentials recorded from the organ of Johnston do not increase continuously with increasing amplitude of antennal vibrations. The potentials are relatively high just above threshold, smaller at vibration-amplitudes of 0,1° and increase beyond this minimum again (Abb. 9, 10).7.The action potentials depend on both the antennal vibrations and the mean steady position of the pedicel-funicle joint (Abb. 14, 15, 17). Particularly lateral or median rotations of the vibrating funicle with respect to the pedicel cause characteristic changes in the pattern of excitation (Abb. 18, 19).8.Behavioural investigations reveal that locus of the antennal vibration (i.e. the position of the pedicel-funicle joint), not its amplitude, provides the final information for the perception of flight speed (Abb. 20).Zusammenfassung1.Niederfrequente Antennenbewegungen (10–20 Hz) während des Fluges, deren. Amplitude ungefähr ±2,5° beträgt, werden aktiv im Seapus-Pedioellus- Gelenk ausgeführt.2.Während der Anströmung mit dem Windkanal treten außerdem schwächere niederfrequente Antennenbewegungen auf, die durch Schwankungen der Anströmgeschwindigkeit verursacht werden.3.Den aktiven Antennenbewegungen sind im Flug passive Drehschwingungen von Arista und Funiculus gegenüber dem Pedicellus („Antennenschwingungen“) überlagert, die die adäquaten mechanischen Reize für den phasischen Luftströmungsrezeptor des Pedicellus, das Johnstonsche Organ, erzeugen. Die Antennenschwingungen werden durch den Flugton (Schallschnelle ≦6 cm/sec) angeregt und haben daher die gleiche Frequenz wie der Flügelschlag.4.Die mechanische Resonanzfrequenz der Antenne liegt ohne Anströmung bei 280 Hz (♀♀) bzw. 350 Hz (♂♂), also deutlich höher als die Flügelschlagfrequenz (Abb. 4). Mit wachsender Dauerauslenkung von Arista und Funiculus bei zunehmender Anströmgeschwindigkeit steigt sie an (Abb. 6), da sich die Federeigensehaften des Pedicellus-Funiculus-Gelenks dabei ändern (Abb. 3). Aus dem gleichen Grunde wird die Schwingungsbreite der Antenne im physiologischen Frequenzbereich mit zunehmender Dauerauslenkung verringert (Abb. 7).5.Das Johnstonsche Organ reagiert am empfindlichsten auf Reizfrequenzen im Bereich der Flügelschlagfrequenz, nämlich bei etwa 200 Hz (Abb. 11–13). Diese maximale Erregung beruht nicht auf der mechanischen Resonanzfrequenz der Antenne, die ja bei weit höheren Frequenzen liegt. Deshalb muß sie auf Eigenschaften des reizleitenden Apparats oder der Sinneszellen selbst beruhen, also auf einer „physiologischen Resonanz“, die der mechanischen Resonanz gegenübergestellt werden kann.6.Die Potentialamplitude des Johnstonschen Organs wächst nicht kontinuierlich mit zunehmender Schwingungsbreite (σ) an, sondern diese Funktion hat bei σ≈0,1° ein deutliches Zwischenminimum (Abb. 10).7.Unter physiologischen Bedingungen hängt die Form der Potentiale des Johnstonschen Organs in komplizierter Weise von Dauerauslenkung und Schwingungsbreite des Funiculus ab (Abb. 14, 15, 17). Während der schwingende Funiculus laterad oder mediad gedreht wird, wie bei einer Änderung der Flugeigengeschwindigkeit, ergibt sich ein besonders charakteristisches Erregungsmuster (Abb. 18, 19).8.Verhaltensversuche zeigen: Nicht die Schwingungsbreite des Funiculus, sondern seine Dauerauslenkung, und damit der Ort der Schwingung, liefert die entscheidende Information für die Wahrnehmung der Flugeigengeschwindigkeit (Abb. 20).

Auditory spatial sensitivity of inferior collicular neurons of echolocating bats

The sensitivity of 94 inferior collicular (IC) neurons of Eptesicus fuscus and Myotis lucifugus to spatial location of the acoustic stimulus were studied under free-field stimulus conditions. The best frequency (BF) and minimum threshold (MT) of each neuron were determined with sound delivered in front of the bat. Then the variation in discharge rate of the neuron was measured with a BF sound broadcast from a moving loudspeaker at different angular positions along the horizontal, vertical or diagonal plane of the frontal auditory space. A wide range of stimulus intensities above the MT of the neuron was used. Neurons were classified into 3 classes on the basis of their spatial sensitivity: (1) omnisensitive neurons (15%) were broadly tuned to sound delivered in the frontal auditory space and their responses did not show any correlation with sound location; (2) stimulus intensity-dependent neurons (28%) varied their discharge rates with sound location and intensity so that the peak of their spatial response profiles also varied with stimulus intensity; and (3) stimulus intensity-independent neurons (57%) varied their discharge rates only with sound location over a wide range of stimulus intensities so that their peak discharge always appeared at the same or a small range of angle. In most cases, the medial limbs of the spatial sensitivity curve for these neurons were extremely sharp and congruent. By moving the loudspeaker along the horizontal, vertical and diagonal planes, it was possible to approximate the boundary of the spatial response area of a neuron. Most IC neurons responded to sound delivered within 20 degrees ipsilateral, 60 degrees contralateral, 45 degrees up and 40 degrees down of the frontal auditory space, confirming previous similar studies. In general, an increasing stimulus repetition rate appeared to sharpen the spatial sensitivity curve of a neuron. Conversely, an increasing moving velocity of the stimulus decreased its response. The possible role of these 3 classes of neurons in echolocation and neural mechanisms underlying the spatial sensitivity of these neurons is discussed.

Calibrated earphones for the echolocating bat,Rhinolophus ferrumequinum

SummaryA method to construct and calibrate earphones (“physiologically”) suitable for small bats and probably other small mammals is described. Particular emphasis was placed on getting a flat frequency response curve between 75kHz and 110kHz, the most important range forRhinolophus ferrumequinum. Below 60kHz the slope declined by about 30dB down to the audible frequency range. The maximal output without harmonic distortion (30dB down) was 80–90dB SPL, but up to 115dB SPL could be attained when accepting harmonics.

Neurons in the cerebellum of echolocating bats respond to acoustic signals

Single neurons responding to auditory stimuli (40 msec duration, 0.5 msec rise-decay time) could be isolated from rather large areas of the cerebellar vermis and hemispheres of an echolocating bat, Eptesicus fuscus. These neurons had latencies between 4 and 13 msec and best frequencies between 22 and 77 kHz. The Q10-dB values of their tuning curves were between 1.4 and 16.6. When acoustic stimuli were delivered though the earphones, tuning curves measured from each ear alone were nearly identical in shape and best frequency. The minimum thresholds of these neurons were between 12 and 65 dB SPL. Apparently, these are suitable for reception of the bats echolocating signals.

Die Leistungen eines Gelenkrezeptors der Antenne von Calliphora für die Perzeption von Luftströmungen. Elektrophysiologische Untersuchungen

Summary1.By means of a stereotactic preparation-technique it was possible to record impulselike action-potentials and receptor-potentials extracellularly from the cell-body or from the axon of a single joint-receptor in the pedicell of the blowfly (Figs. 2, 10). Most probably this receptor is identical with the sensillum campaniforme, described by Gewecke (1967 a, b) (Fig. 1).2.The sense cell of this receptor reacts to passive torsion of the funiculus against the pedicell with phasic-tonically dischargepatterns, if the displacement is laterally directioned (Figs. 2, 10). This is the physiological stimulus which is normally caused by aircurrents e.g. during the flight. A torsion of the funiculus from its resting position in the other direction (median displacement) does not change the spontaneous frequency. But if the funiculus returns from a lateral displacement to a more median position, dischargepatterns which are like mirror images of those caused by excitation will result: at first the frequency decreases or disappears completely and then increases again to a new level (Fig. 13 and Schlegel, 1968).3.When caused by an exciting stimulus the impulse-frequency overshoots instantaneously and then falls quickly from the maximum to the plateaufrequency (Figs. 3, 4). This “adaption” surely does not depend on a diminution of the excitability of the sense cell but indicates the dynamic response of the receptor.4.Under rectangular time course stimuli, the height of the overshoot and the plateau-frequency are linearely correlated with the stimulus strength (displacement of the funiculus). The working range of the receptor includes about 12° (angle of the funiculus torsion (Figs. 6, 7).5.The physiologically most important range of the pedicell-funiculus-joint lies according to behavioural investigations between 2° and 5°. Within the same range the receptors excitability to stimulus-changes is also highest (Figs. 7, 8).6.Velocity as a parameter of stimulus: The phasic response depends linearly on the logarithm of stimulus speed. Saturation of the overshoot is observed when the speed exceeds approximately 100°/sec (Figs. 11, 13, 14).7.With respect to periodic stimuli (rectangular and sinoidal) the receptor reacts with excitation to lateral movements and with inhibition to median movements. Between about 100 and 250 Hz the ratio between stimulus and impulse frequency is, within a wide range, independent of the stimulus amplitude and the displacement (position), and is 1∶1 (Figs. 9, 15). The impulses are synchronized sharply with the stimuli.8.During fixed flight the displacement of the arista is superimposed by vibrations caused by the sound of the animals own wingstroke. Their amplitudes are in the range of normal flight speeds, reduced in such a manner (ca. 0.2°) that they never exceed the threshold of the receptor (Fig. 16). But the amplitude is sufficient for exciting the Johnstons organ; this might be important for regulating the wingbeat.9.The electrophysiological evidence suggests that the pedicell-funiculus-joint possesses besides the phasic receptor-system of the Johnstons organ also a tonic receptor-system, constituted by a single cell, which is able to measure the funiculus position. This receptor could give information which is necessary for the active antennal movements.Zusammenfassung1.Eine stereotaktische Ableittechnik ermöglicht es, extracellulär Aktionspotentiale vom Sinneszellkörper oder vom proximalen Teil des Axon eines einzelnen Gelenkrezeptors in der Antenne von Calliphora vicina abzuleiten. Sehr wahrscheinlich ist der Rezeptor identisch mit dem von Gewecke (1967a, b) beschriebenen Sensillum campaniforme.2.Der Rezeptor reagiert auf die passive und einzig mögliche, laterade Drehung des Funiculus gegenüber dem Pedicellus — dem normalen physiologischen Reiz — mit phasisch-tonischer Erregung. Eine mediade Drehung des Funiculus verändert die Ruhefrequenz nicht. Beim Rückdrehen des Funiculus von einer Dauerauslenkung entstehen zur Erregung etwa reziproke Entladungsmuster (Frequenzabfall bzw. Impulspause und Wiederanstieg zu einer anderen Dauerfrequenz).3.Der Erregungsabfall von der Spitzenfrequenz zur Plateaufrequenz erfolgt relativ rasch (Halbwertszeit des Frequenzabfalls unabhängig von Reizamplitude und Höhe der Spitzenfrequenz rund 300 msec). Der Erregungsabfall ist keine Adaptation (Empfindlichkeitsminderung).4.Die Höhe der phasischen (Spitzenfrequenz) und der tonischen (Plateaufrequenz) Erregung der Sinneszelle hängt bei rechteckförmigen Einzelreizen etwa linear von der Reizstärke (Drehwinkel des Funiculus) ab. Der Arbeitsbereich des Rezeptors umfaßt etwa 12° Funiculusdrehung. Die tonische „Meßgenauigkeit“ beträgt 0,5–1°.5.Der physiologisch wichtigste Arbeitsbereich des Gelenks liegt bei Verhaltensversuchen zwischen 2 und 5°. In diesem Bereich ist die Empfindlichkeit des Rezeptors für Reizänderungen am größten (Treppenreizversuche).6.Parameter Reizgeschwindigkeit: die phasische Erregung hängt linear vom Logarithmus der Anstiegsgeschwindigkeit des Reizes ab. Bei Reizanstiegsgeschwindigkeiten über etwa 100°/sec erreicht der Wert der Spitzenfrequenz den für jede Reizamplitude höchstmöglichen Wert (Sättigung).7.Bei periodischen Reizen (Rechteck oder Sinus) reagiert die Sinneszelle auf die jeweils laterade Drehphase mit Erregung, auf die mediade mit Impulspausen. Zwischen etwa 100 und 250 Hz herrscht weitgehend unabhängig von Schwingungsbreite und Dauerauslenkung des Reizes ein Verhältnis von 1∶1 zwischen Reiz- und Impulsfrequenz vor. Die Impulse werden streng synchron mit den Reizen ausgelöst.8.Die im fixierten Flug der Dauerauslenkung der Aristen überlagerten Sinus schwingungen, die vom Schall des eigenen Flügelschlags angeregt werden (Gewecke und Schlegel, 1968), sind für den Rezeptor nicht überschwellig. Die Schwingungsbreite reicht aber aus, um das Johnstonsche Organ zu erregen; das dürfte für die Steuerung des Flügelschlags von entscheidender Bedeutung sein.9.Somit ist auch elektrophysiologisch bewiesen, daß das Pedicellus-Funiculus-Gelenk neben dem phasisch reagierenden Johnstonschen Organ auch einen tonischen Rezeptor für absolute Winkelmessungen (Stellung) besitzt. Der Rezeptor könnte die Informationen für die aktive Antenneneinstellung (Bereichseinstellung) liefern.

Unmasking in neurons of the inferior colliculus of Eptesicus fuscus with binaural stimulation

171 single inferior colliculus neurons displaying basic auditory properties similar to those described previously were sampled, and 118 of those were tested to determine whether monaurally masked responses (band passed noise of +/- 5 kHz around the best frequency of the pure tone) could be recovered if the masking noise was presented binaurally. 26% of the units tested showed such an improvement in signal detection, i.e. what is called masking level difference (MLD) by psychoacousticians. Signal detection was improved by more than 20 dB in a few cases, but the usual improvement did not exceed 11 dB. The data suggest that MLD occurs only in units showing binaural facilitation in addition to inhibition (I, E/E type), in contrast to the more common binaural I/E types which may only provide basic azimuth information. The neurophysiological results are discussed in view of the findings described in the literature on psychoacoustical MLD and in terms of the biological importance these results have for the bats acoustical space orientation (echolocation) and this systems excellent resistance to jamming. Since psychoacoustical explanations for the MLD effect appear to be of little relevance on a cellular level, possible neural mechanisms are discussed as well.

Einzelableitungen von einem Stellungsrezeptor im Pedicellus-Funiculus-Gelenk des blauen Brummers (Calliphora vicina Rob. Desv., erythrocephala auct.)

Summary1.Recordings from a position receptor in the pedicellus-funiculus joint of the blowfly (Calliphora vicinaRob. Desv.) are described.2.The recorded potentials originate most likely from the single sensillum campaniforme situated near that joint.3.The receptor reacts phasic-tonically to torsions of the funiculus in respect to the pedicellus.4.The steady state frequencies of discharge increase nearly linearly with the stimulus amplitude until the catch of the joint is reached, but do not depend upon the angular speed of the stimulus or the manner how the position was reached.5.The dynamic part of the receptor discharge increases linearly with the logarithm of the angular speed within the range of very slow torsion velocities. With faster angular velocities the dynamic response does not change with angular speed (provided that the stimulus amplitude is constant). The dynamic response depends under these conditions only on the stimulus amplitude.6.The receptor reacts so slowly that funiculus-oscillations of frequencies, which are somewhat below wingbeat frequency and are superimposed to a steady torsion, barely are resolved. Such high frequencies of oscillation, which may occur during flight, therefore probabely do not disturb position measuring.Zusammenfassung1.Ableitungen von einem Stellungsrezeptor im Pedicellus-Funiculus-Gelenk der Fliege Calliphora vicina, Rob. Desv. werden beschrieben.2.Die Registrierungen stammen wahrscheinlich von dem in diesem Gelenk gelegenen, einzelnen Sensillum campaniforme, dessen Bau Gewecke (1964, 1967 und im Druck) untersucht hat.3.Der Rezeptor reagiert auf Auslenkungen des Funiculus gegenüber dem Pedicellus phasisch-tonisch.4.Die stationäre Impulsfrequenz hängt bis zum Erreichen des Gelenkanschlags etwa linear von der Reizamplitude ab. Sie ist unabhängig von der Reizanstiegssteilheit und dem Weg, auf dem die Stellung erreicht wurde.5.Die phasische Reaktion des Rezeptors hängt bei sehr langsamen Drehungen linear vom Logarithmus der Anstiegssteilheit ab. Bei schnelleren Drehungen ändert sich die phasische Antwort bei konstanter Endauslenkung nicht mehr mit der Drehgeschwindigkeit. Sie hängt dann nur noch von der Reizamplitude ab.6.Der Rezeptor reagiert so träge, daß schon Schwingungen des Funiculus mit Frequenzen, die noch unterhalb der Flügelschlagfrequenz liegen, nur noch schlecht wiedergegeben werden. Solche Schwingungen, die z.B. auch im fixierten Flug einer Dauerauslenkung überlagert sind, stören die Messung der Dauerauslenkung wahrscheinlich kaum.