Philip H.-S. Jen

Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus.

Summary1.Encoding of temporal stimulus parameters by inferior collicular (IC) neurons of Eptesicus fuscus was studied by recording their responses to a wide range of repetition rates (RRs) and durations at several stimulus intensities under free field stimulus conditions.2.The response properties of 424 IC neurons recorded were similar to those reported in previous studies of this species.3.IC neurons were classified as low-pass, band-pass, and high-pass according to their preference for RRs (Fig. 6) and/or durations (Fig. 8) characteristic of, respectively, search, approach, or terminal phases of echolocation. These neurons selectively process stimuli characteristic of the various phases of hunting.4.Best RRs (Fig. 7A) and best durations (Fig. 7B) were not correlated with either the BFs or recording depths (Figs. 7C, D and 10). This suggests that each isofrequency lamina is capable of processing RRs and durations of all hunting phases.5.Responses of one half of IC neurons studied were correlated with the stimulus duty cycle (Fig. 9). These neurons may preferentially process terminal phase information when the bats pulse emission duty cycle increases.6.While the stimulus RR affected the dynamic range and overall profile of the intensity rate function (Fig. 11), only little effect was observed with different stimulus durations (Fig. 12).

Frequency and space representation in the primary auditory cortex of the frequency modulating batEptesicus fuscus

Summary1.Frequency and space representation in the auditory cortex of the big brown bat,Eptesicus fuscus, were studied by recording responses of 223 neurons to acoustic stimuli presented in the bats frontal auditory space.2.The majority of the auditory cortical neurons were recorded at a depth of less than 500 urn with a response latency between 8 and 20 ms (Fig. 1 B, C). They generally discharged phasically and had nonmonotonic intensity-rate functions (Fig. 3). The minimum threshold, (MT) of these neurons was between 8 and 82 dB sound pressure level (SPL). Half of the cortical neurons showed spontaneous activity. All 55 threshold curves are Vshaped and can be described as broad, intermediate, or narrow (Fig. 4A).3.Auditory cortical neurons are tonotopically organized along the anteroposterior axis of the auditory cortex. High-frequency-sensitive neurons are located anteriorly and low-frequency-sensitive neurons posteriorly (Figs. 5, 6). An overwhelming majority of neurons were sensitive to a frequency range between 30 and 75 kHz (Fig. 1 A).4.When a sound was delivered from the response center of a neuron on the bats frontal auditory space, the neuron had its lowest MT. When the stimulus amplitude was increased above the MT, the neuron responded to sound delivered within a defined spatial area. The response center was not always at the geometric center of the spatial response area. The latter also expanded with stimulus amplitude (Fig. 8). High-frequency-sensitive neurons tended to have smaller spatial response areas than low-frequency-sensitive neurons (Figs. 7, 9).5.Response centers of all 223 neurons were located between 0‡ and 50‡ in azimuth, 2‡ up and 25‡ down in elevation of the contralateral frontal auditory space (Fig. 10). Response centers of auditory cortical neurons tended to move toward the midline and slightly downward with increasing best frequency (BF; Fig. 11).6.Auditory space representation appears to be systematically arranged according to the tonotopic axis of the auditory cortex. Thus, the lateral space is represented posteriorly and the middle space anteriorly (Fig. 12). Space representation, however, is less systematic in the vertical direction (Fig. 13).7.Auditory cortical neurons are columnarly organized. Thus, the BFs, MTs, threshold curves, azimuthal location of response centers, and auditory spatial response areas of neurons sequentially isolated from an orthogonal electrode penetration are similar (Figs. 4, 7).

CORTICOFUGAL REGULATION OF AUDITORY SENSITIVITY IN THE BAT INFERIOR COLLICULUS

Abstract Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal interstimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of γ-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway.

Analysis of orientation signals emitted by the CF-FM bat,Pteronotus p. parnellii and the FM bat,Eptesicus fuscus during avoidance of moving and stationary obstacles

Summary1.The echolocative skills ofPteronotus parnellii parnellii andEptesicus fuscus were studied by measuring their ability in avoiding stationary and moving obstacles.2.The frequency, repetition rate, duration and amplitude of the orientation signals emitted by the bat during three phases of negotiation of obstacles were studied.3.During the avoidance of obstacles, both species of bats systematically shorten the duration, increase the repetition rate, and decrease the amplitude of their emitted orientation signals as they approach, negotiate and pass the obstacles.4.Flying at different speeds inside the flight room during the avoidance of obstacles,Pteronotus parnellii parnellii appropriately adjust their emitted CF frequency according to the flight speed to accurately compensate for the positively Doppler-shifted echoes.5.The frequency of the FM signals emitted at high repetition rate byEptesicus fuscus shifts downward as the bat enters into the final phase of negotiation of the obstacles.6.The significance of the change in parameters of emitted signals in relation to echolocation is discussed. Presumably, the increase in the repetition rate of sound emission and the shortening of the sound duration is to monitor rapid changes in obstacle positions. The decrease in sound amplitude is either due to the difficulty in producing loud short sounds at the end of a long-held breath or to appropriately adjust the echo amplitude into the optimal range of sensitivity of the bats ears.

Bicuculline application affects discharge patterns, rate–intensity functions, and frequency tuning characteristics of bat auditory cortical neurons

This study examined the effect of bicuculline application on the auditory response properties in the auditory cortex of the big brown bat, Eptesicus fuscus. All auditory cortical neurons studied discharged either 1-2 or 3-7 impulses to 4 ms sound stimuli. Cortical neurons with high best frequencies tended to have high minimum thresholds. Bicuculline application increased the number of impulses and shortened the response latencies of all cortical neurons as well as changing the discharge patterns of half of the cortical neurons studied. Bicuculline application raised the rate-intensity functions but lowered the latency-intensity functions to varying degrees. Threshold-frequency tuning curves (FTCs) were either V-shaped, upper threshold or double-peaked. Threshold-FTCs and impulse-FTCs were mirror-images of each other. Bicuculline application expanded and raised the impulse-FTCs but lowered the threshold-FTCs, resulting in significantly decreased Q(n) values. Threshold-FTCs of cortical neurons determined within an orthogonally inserted electrode were very similar and expanded FTCs during bicuculline application were also very similar. Possible mechanisms for the contribution of GABAergic inhibition to shaping these response properties of cortical neurons are discussed.

Directionality of sound pressure transformation at the pinna of echolocating bats.

The directionality of sound pressure transformation at the pinna of three species of bats was studied by measuring the sound pressure level of a tone (25 45 65 and 85 kHz) at the tympanic membrane as a function of azimuth and elevation of the sound source under free-field conditions. The tympanic sound pressure level varied with location of the sound source. The directionality of sound pressure transformation pattern of the pinna of each bat was studied by plotting isopressure contours. The area within each isopressure contour decreased with increasing tonal frequency. For each tonal frequency, the point of maximal sound pressure was always located in the frontal ipsilateral sound field. This point shifted medially with increasing tonal frequency along the horizontal plane in all species tested, but it shifted in a species-specific manner along the vertical plane. Removal or distortion of the pinna and tragus resulted in either uncircumscribed or irregular isopressure contours for all tonal frequencies tested. Acoustic pressure gain of the external ear reached 16-23 dB for frequencies at 15-18 kHz. The importance of the external ear to the directionality of the bats echolocation system is discussed.

Corticofugal influences on the responses of bat inferior collicular neurons to sound stimulation

Corticofugal influences on the responses of inferior collicular neurons (IC) to acoustic stimulation were studied by electrical stimulation of the auditory cortex. Among 471 IC neurons isolated, about 26% were affected by cortical stimulation. Responses of 103 (22%) IC neurons were inhibited and 17 (3.6%) were facilitated. The degree of inhibition was dependent upon the amplitude of both auditory and electrical stimuli. Corticofugal inhibition of the response of an IC neuron was likely due to an increase in the neurons minimum threshold. Inhibitory latency varied with the interstimulus interval. The shortest inhibitory latency of most IC neurons was between 1 and 2 ms. The localization of the point of cortical stimulation was crucial in determining the responses of IC neurons. It is assumed that corticofugal influences on IC neurons are a part of regulatory mechanism in the centrifugal pathway for frequency analysis and acoustic orientation.

Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus.

The auditory spatial response areas of 333 inferior collicular (IC) neurons of Eptesicus fuscus were studied under free-field acoustic stimulus conditions. A stimulus was delivered from a loudspeaker placed 14 cm in front of a bat and the best frequency of an encountered neuron was determined. Then a best frequency (BF) stimulus was delivered as the loudspeaker was moved across the frontal auditory space to determine the response center of the neuron. At the response center, the neuron had the lowest minimum threshold. The stimulus was then raised 3-15 dB above the lowest minimum threshold of the neuron and the spatial response area for each stimulus intensity was measured. The response center and spatial response area of a neuron measured with a one-octave downward-sweep FM stimulus were similar to those measured with the pure tone pulse. The spatial response area of a neuron expanded asymmetrically with the stimulus intensity. High BF neurons generally had smaller spatial response areas than low BF neurons had. All 333 response centers were located in the contralateral auditory space. Response centers of low BF neurons tended to be located laterally while those of high BF neurons were located medially. Although each neuron had a point of lowest minimum threshold in the contralateral auditory space, the point-to-point representation of the auditory space was not systematically organized. This representation was not correlated with the recording sites of the neurons in the mediolateral, posteroanterior and dorsoventral axes of the IC.

An electrophysiological study of neural pathways for corticofugally inhibited neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus

Abstract. This electrophysiological study tests the hypothesis that one possible neural pathway for corticofugally inhibited neurons in the central nucleus of the inferior colliculus (ICc) of the big brown bat, Eptesicus fuscus, is mediated through excitatory projections from the auditory cortex (AC) to the external nucleus of the IC (ICx), which then sends inhibitory inputs to the ICc. This study shows that all neurons in the ICx are broadly tuned to stimulus frequency. Electrical stimulation in the AC typically increases the number of impulses, expands the auditory spatial response areas, and broadens the frequency tuning curves (FTCs) of neurons in the ICx. This corticofugal facilitation is mediated at least in part through NMDA receptors, since application of DL-2-amino-5-phosphonovaleric acid (APV), an antagonist for NMDA, decreases these response properties of neurons in the ICx. Electrical stimulation in the ICx typically decreases the number of impulses, reduces the auditory spatial response areas, and narrows the FTCs of neurons in the ICc. This inhibition is mediated at least in part through GABAA receptors, since application of bicuculline, an antagonist for GABA, increases these response properties of neurons in the ICc. These data suggest that corticofugal facilitation of the ICx and the inhibition of the ICx to the ICc may be one of the polysynaptic pathways for corticofugal inhibition of neurons in the ICc. Possible functions of this polysynaptic pathway in acoustic orientation and signal processing are discussed.

GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons

Abstract. This study examined the effect of GABAergic and glycinergic inhibition on excitatory frequency tuning curves (FTCs) of inferior collicular (IC) neurons of the big brown bat, Eptesicus fuscus. The excitatory FTCs of 70 IC neurons were either V-shaped (57, 81%), closed (11, 16%), or double-peaked (2, 3%). By means of a two-tone stimulation paradigm, inhibitory FTCs were obtained at one frequency flank only (low-frequency flank: 11, 16%; high-frequency flank: 7, 10%), at both frequency flanks (36, 51%) of excitatory FTCs, or between two excitatory FTCs (2, 3%). IC neurons that had inhibitory FTCs typically had larger Q10 and Q30 values (i.e., sharper excitatory FTCs) than neurons that did not have inhibitory FTCs. Neurons with inhibitory FTCs at both frequency flanks had larger Q10 and Q30 values than neurons with inhibitory FTCs at one frequency flank only. IC neurons with a small difference between excitatory and inhibitory best frequencies typically had sharper excitatory frequency tuning. Bicuculline (an antagonist for GABAA) application produced a greater degree of abolishing inhibitory FTCs than strychnine (an antagonist for glycine) application. Application of both drugs was most effective in abolishing the inhibitory FTCs of IC neurons. The implications of these findings for bat echolocation are discussed.