Single cortical neurons serve both echolocation and passive sound localization.
The pallid bat uses passive listening at low frequencies to detect and locate terrestrial prey and reserves its high-frequency echolocation for general orientation. While hunting, this bat must attend to both streams of information. These streams are processed through two parallel, functionally specialized pathways that are segregated at the level of the inferior colliculus. This report describes functionally bimodal neurons in auditory cortex that receive converging input from these two pathways. Each brain stem pathway imposes its own suite of response properties on these cortical neurons. Consequently, the neurons are bimodally tuned to low and high frequencies, and respond selectively to both noise transients used in prey detection, and downward frequency modulation (FM) sweeps used in echolocation. A novel finding is that the monaural and binaural response properties of these neurons can change as a function of the sound presented. The majority of neurons appeared binaurally inhibited when presented with noise but monaural or binaurally facilitated when presented with the echolocation pulse. Consequently, their spatial sensitivity will change, depending on whether the bat is engaged in echolocation or passive listening. These results demonstrate that the response properties of single cortical neurons can change with behavioral context and suggest that they are capable of supporting more than one behavior. (+info
Echolocation behaviour and prey-capture success in foraging bats: laboratory and field experiments on Myotis daubentonii.
During prey-capture attempts, many echolocating bats emit a 'terminal buzz', when pulse repetition rate is increased and pulse duration and interpulse interval are shortened. The buzz is followed by a silent interval (the post-buzz pause). We investigated whether variation in the structure of the terminal buzz, and the calls and silent periods following it, may provide information about whether the capture attempt was successful and about the size of prey detected - detail that is valuable in studies of habitat use and energetics. We studied the trawling bat Myotis daubentonii. The time between the first call of the approach phase and the end of the terminal phase was not related to prey size in the laboratory. The last portion of the terminal buzz (buzz II) was shortened or omitted during aborted capture attempts. Both in the laboratory and in the field, the mean interpulse interval immediately after the terminal buzz (post-buzz interpulse interval) was longer in successful captures than in unsuccessful attempts. In the laboratory, the post-buzz pause was longer after successful captures than for unsuccessful attempts, and the minimum frequency of the first search-phase call emitted after the buzz (Fmin) was higher than that of the last such call prior to the buzz. These effects were not apparent in field data. Both in the laboratory (85%) and in the field (74%), significant discrimination between successful and unsuccessful capture attempts was possible when the duration of the post-buzz pause, post-buzz interpulse interval and Fmin were entered into a discriminant analysis. Thus, variation in the echolocation calls of bats during prey-capture attempts can reveal substantial information about capture success and prey size. (+info
Multiple components of ipsilaterally evoked inhibition in the inferior colliculus.
The central nucleus of the inferior colliculus (ICc) receives a large number of convergent inputs that are both excitatory and inhibitory. Although excitatory inputs typically are evoked by stimulation of the contralateral ear, inhibitory inputs can be recruited by either ear. Here we evaluate ipsilaterally evoked inhibition in single ICc cells in awake Mexican free-tailed bats. The principal question we addressed concerns the degree to which ipsilateral inhibition at the ICc suppresses contralaterally evoked discharges and thus creates the excitatory-inhibitory (EI) properties of ICc neurons. To study ipsilaterally evoked inhibition, we iontophoretically applied excitatory neurotransmitters and visualized the ipsilateral inhibition as a gap in the carpet of background activity evoked by the transmitters. Ipsilateral inhibition was seen in 86% of ICc cells. The inhibition in most cells had both glycinergic and GABAergic components that could be blocked by the iontophoretic application of bicuculline and strychnine. In 80% of the cells that were inhibited, the ipsilateral inhibition and contralateral excitation were temporally coincident. In many of these cells, the ipsilateral inhibition suppressed contralateral discharges and thus generated the cell's EI property in the ICc. In other cells, the ipsilateral inhibition was coincident with the initial portion of the excitation, but the inhibition was only 2-4 ms in duration and suppressed only the first few contralaterally evoked discharges. The suppression was so slight that it often could not be detected as a decrease in the spike count generated by increasing ipsilateral intensities. Twenty percent of the cells that expressed inhibition, however, had inhibitory latencies that were longer than the excitatory latencies. In these neurons, the inhibition arrived too late to suppress most or any of the discharges. Finally, in the majority of cells, the ipsilateral inhibition persisted for tens of milliseconds beyond the duration of the signal that evoked it. Thus ipsilateral inhibition has multiple components and one or more of these components are typically evoked in ICc neurons by sound received at the ipsilateral ear. (+info
Micromechanical responses to tones in the auditory fovea of the greater mustached bat's cochlea.
An extended region of the greater mustached bat's cochlea, the sparsely innervated (SI) zone, is located just basally to the frequency place of the dominant 61-kHz component of the echolocation signal (CF2). Anatomic adaptations in the SI zone are thought to provide the basis for cochlear resonance to the CF2 echoes and for the extremely sharp tuning throughout the auditory system that allows these bats to detect Doppler shifts in the echoes caused by insect wing beat. We measured basilar membrane (BM) displacements in the SI zone with a laser interferometer and recorded acoustic distortion products at the ear drum at frequencies represented in the SI zone. The basilar membrane in the SI region was tuned both to its characteristic frequency (62-72 kHz) and to the resonance frequency (61-62 kHz). With increasing stimulus levels, the displacement growth functions are compressive curves with initial slopes close to unity, and their properties are consistent with the mammalian cochlear amplifier working at high sound frequencies. The sharp basilar membrane resonance is associated with a phase lag of 180 degrees and with a shift of the peak resonance to lower frequencies for high stimulus levels. Within the range of the resonance, the distortion product otoacoustic emissions, which have been attributed to the resonance of the tectorial membrane in the SI region, are associated with an abrupt phase change of 360 degrees. It is proposed that a standing wave resonance of the tectorial membrane drives the BM in the SI region and that the outer hair cells enhance, fine tune, and control the resonance. In the SI region, cochlear micromechanics appear to be able to work in two different modes: a conventional traveling wave leads to shear displacement between basilar and tectorial membrane and to neuronal excitation for 62-70 kHz. In addition, the SI region responds to 61-62 kHz with a resonance based on standing waves and thus preprocesses signals which are represented more apically in the CF2 region of the cochlea. (+info
Delay-tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance.
We examined response properties of delay-tuned neurons in the central nucleus of the inferior colliculus (ICC) of the mustached bat. In the mustached bat, delay-tuned neurons respond best to the combination of the first-harmonic, frequency-modulated (FM1) sweep in the emitted pulse and a higher harmonic frequency-modulated (FM2, FM3 or FM4) component in returning echoes and are referred to as FM-FM neurons. We also examined H1-CF2 neurons. H1-CF2 neurons responded to simultaneous presentation of the first harmonic (H1) in the emitted pulse and the second constant frequency (CF2) component in returning echoes. These neurons served as a comparison as they are thought to encode different features of sonar targets than FM-FM neurons. Only 7% of our neurons (14/198) displayed a single excitatory tuning curve. The rest of the neurons (184) displayed complex responses to sounds in two separate frequency bands. The majority (51%, 101) of neurons were facilitated by the combination of specific components in the mustached bat's vocalizations. Twenty-five percent showed purely inhibitory interactions. The remaining neurons responded to two separate frequencies, without any facilitation or inhibition. FM-FM neurons (69) were facilitated by the FM1 component in the simulated pulse and a higher harmonic FM component in simulated echoes, provided the high-frequency signal was delayed the appropriate amount. The delay producing maximal facilitation ("best delay") among FM-FM neurons ranged between 0 and 20 ms, corresponding to target distances +info)
Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats.
Mustached bats, Pteronotus parnellii parnellii, emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF(1-4)) component followed by a short, frequency-modulated (FM(1-4)) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF(2) is maintained within a narrowband centered at approximately 61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63. 0-kHz frequencies in the "Doppler-shifted CF processing" (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of approximately 25 kHz (BF(low)) and approximately 61 kHz (BF(high)). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BF(low) corresponding to a frequency in the lower half of the echolocation pulse FM(1) sweep and another of sharp tuning to frequencies centered at BF(high) corresponding to the CF(2) in the echo. Facilitative response areas for BF(high) are broadened by approximately 0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BF(high) response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BF(high). About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BF(high) so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BF(high) and sometimes for BF(low). Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area. (+info
Scaling of echolocation call parameters in bats.
I investigated the scaling of echolocation call parameters (frequency, duration and repetition rate) in bats in a functional context. Low-duty-cycle bats operate with search phase cycles of usually less than 20 %. They process echoes in the time domain and are therefore intolerant of pulse-echo overlap. High-duty-cycle (>30 %) species use Doppler shift compensation, and they separate pulse and echo in the frequency domain. Call frequency scales negatively with body mass in at least five bat families. Pulse duration scales positively with mass in low-duty-cycle quasi-constant-frequency (QCF) species because the large aerial-hawking species that emit these signals fly fast in open habitats. They therefore detect distant targets and experience pulse-echo overlap later than do smaller bats. Pulse duration also scales positively with mass in the Hipposideridae, which show at least partial Doppler shift compensation. Pulse repetition rate corresponds closely with wingbeat frequency in QCF bat species that fly relatively slowly. Larger, fast-flying species often skip pulses when detecting distant targets. There is probably a trade-off between call intensity and repetition rate because 'whispering' bats (and hipposiderids) produce several calls per predicted wingbeat and because batches of calls are emitted per wingbeat during terminal buzzes. Severe atmospheric attenuation at high frequencies limits the range of high-frequency calls. Low-duty-cycle bats that call at high frequencies must therefore use short pulses to avoid pulse-echo overlap. Rhinolophids escape this constraint by Doppler shift compensation and, importantly, can exploit advantages associated with the emission of both high-frequency and long-duration calls. Low frequencies are unsuited for the detection of small prey, and low repetition rates may limit prey detection rates. Echolocation parameters may therefore constrain maximum body size in aerial-hawking bats. (+info
Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats.
The big brown bat, Eptesicus fuscus, navigates and hunts prey with echolocation, a modality that uses the temporal and spectral differences between vocalizations and echoes from objects to build spatial images. Closely spaced surfaces ("glints") return overlapping echoes if two echoes return within the integration time of the cochlea ( approximately 300-400 micros). The overlap results in spectral interference that provides information about target structure or texture. Previous studies have shown that two acoustic events separated in time by less than approximately 500 micros evoke only a single response from neural elements in the auditory brain stem. How does the auditory system encode multiple echoes in time when only a single response is available? We presented paired FM stimuli with delay separations from 0 to 24 micros to big brown bats and recorded local field potentials (LFPs) and single-unit responses from the inferior colliculus (IC). These stimuli have one or two interference notches positioned in their spectrum as a function of two-glint separation. For the majority of single units, response counts decreased for two-glint separations when the resulting FM signal had a spectral notch positioned at the cell's best frequency (BF). The smallest two-glint separation that reliably evoked a decrease in spike count was 6 micros. In addition, first-spike latency increased for two-glint stimuli with notches positioned nearby BF. The N(4) potential of averaged LFPs showed a decrease in amplitude for two-glint separations that had a spectral notch near the BF of the recording site. Derived LFPs were computed by subtracting a common-mode signal from each LFP evoked by the two-glint FM stimuli. The derived LFP records show clear changes in both the amplitude and latency as a function of two-glint separation. These observations in relation with the single-unit data suggest that both response amplitude and latency can carry information about two-glint separation in the auditory system of E. fuscus. (+info