Mustached Bat Research Articles

Directional selectivity for FM sweeps in the suprageniculate nucleus of the mustached bat medial geniculate body.

Mustached bats emit echolocation and communication calls containing both constant frequency (CF) and frequency-modulated (FM) components. Previously we found that 86% of neurons in the ventral division of the external nucleus of the inferior colliculus (ICXv) were directionally selective for linear FM sweeps and that selectivity was dependent on sweep rate. The ICXv projects to the suprageniculate nucleus (Sg) of the medial geniculate body. In this study, we isolated 37 single units in the Sg and measured their responses to best excitatory frequency (BEF) tones and linear 12-kHz upward and downward FM sweeps centered on the BEF. Sweeps were presented at durations of 30, 12, and 4 ms, yielding modulation rates of 400, 1,000, and 3,000 kHz/s. Spike count versus level functions were obtained at each modulation rate and compared with BEF controls. Sg units responded well to both tones and FM sweeps. BEFs clustered at 58 kHz, corresponding to the dominant CF component of the sonar signal. Spike count functions for both tones and sweeps were predominantly non-monotonic. FM directional selectivity was significant in 53-78% of the units, depending on modulation rate and level. Units were classified as up-selective (52%), down-selective (24%), or bi-directional (non-selective, 16%); a few units (8%) showed preferences that were either rate- or level-dependent. Most units showed consistent directional preferences at all SPLs and modulation rates tested, but typically showed stronger selectivity at lower sweep rates. Directional preferences were attributable to suppression of activity by sweeps in the non-preferred direction (~80% of units) and/or facilitation by sweeps in the preferred direction (~20-30%). Latencies for BEF tones ranged from 4.9 to 25.7 ms. Latencies for FM sweeps typically varied linearly with sweep duration. Most FM latency-duration functions had slopes ranging from 0.4 to 0.6, suggesting that the responses were triggered by the BEF. Latencies for BEF tones and FM sweeps were significantly correlated in most Sg units, i.e., the response to FM was temporally related to the occurrence of the BEF in the FM sweep. FM latency declined relative to BEF latency as modulation rate increased, suggesting that at higher rates response is triggered by frequencies in the sweep preceding the BEF. We conclude that Sg and ICXv units have similar, though not identical, response properties. Sg units are predominantly upsweep selective and could respond to either or both the CF and FM components in biosonar signals in a number of echolocation scenarios, as well as to a variety of communication sounds.

Excitatory and facilitatory frequency response areas in the inferior colliculus of the mustached bat

In the mustached bat’s central nucleus of the inferior colliculus (ICC), many neurons display facilitatory or inhibitory responses when presented with two tones of distinctly different frequencies. Our previous studies have focused on spectral interactions between specific frequency bands contained in the bat’s sonar vocalization. In this study, we describe excitatory and facilitatory frequency response areas across all frequencies in the mustached bat’s audible range. We show that many neurons in the ICC have more extensive frequency interactions than previously documented. We recorded responses of 96 single units to single tones and combinations of two tones. Best frequencies of the units ranged from 59-15 kHz. Forty-one units had a single, excitatory frequency response area. The rest of the units had more complex frequency tuning that included multiple excitatory frequency response areas and facilitatory frequency response areas. Some of the facilitatory frequency interactions were between one sound with energy in a sonar frequency band and a second sound with energy in a non-sonar frequency band. We also found that neurons could be facilitated by more than one additional frequency band. Our findings of extensive frequency interactions in the ICC of the mustached bat suggest that some neurons may be well suited for the analysis of complex sounds, possibly including social communication sounds.

Erratum: Modulation of cochlear hair cells by the auditory cortex in the mustached bat

Erratum: Modulation of cochlear hair cells by the auditory cortex in the mustached bat

Modulation of cochlear hair cells by the auditory cortex in the mustached bat.

The corticofugal (descending) auditory system forms multiple feedback loops, and adjusts and improves auditory signal processing in the subcortical auditory nuclei. However, the mechanism by which the corticofugal system modulates cochlear hair cells has been unexplored. We found that electric stimulation of cortical neurons via the corticofugal system modulates cochlear hair cells in a highly specific way according to the relationship in terms of best frequency between cortical neurons and hair cells. Such frequency-specific effects can be explained by selective corticofugal modulation of individual olivocochlear efferent fibers.

Medial superior olive of the big brown bat: neuronal responses to pure tones, amplitude modulations, and pulse trains.

The structure and function of the medial superior olive (MSO) is highly variable among mammals. In species with large heads and low-frequency hearing, MSO is adapted for processing interaural time differences. In some species with small heads and high-frequency hearing, the MSO is greatly reduced in size; in others, including those echolocating bats that have been examined, the MSO is large. Moreover, the MSO of bats appears to have undergone different functional specializations depending on the type of echolocation call used. The echolocation call of the mustached bat contains a prominent CF component, and its MSO is predominantly monaural; the free-tailed bat uses pure frequency-modulated calls, and its MSO is predominantly binaural. To further explore the relation of call structure to MSO properties, we recorded extracellularly from 97 single neurons in the MSO of the big brown bat, Eptesicus fuscus, a species whose echolocation call is intermediate between that of the mustached bat and the free-tailed bat. The best frequencies of MSO neurons in the big brown bat ranged from 11 to 79 kHz, spanning most of the audible range. Half of the neurons were monaural, excited by sound at the contralateral ear, while the other half showed evidence of binaural interactions, supporting the idea that the binaural characteristics of MSO neurons in the big brown bat are midway between those of the mustached bat and the free-tailed bat. Within the population of binaural neurons, the majority were excited by sound at the contralateral ear and inhibited by sound at the ipsilateral ear; only 21% were excited by sound at either ear. Discharge patterns were characterized as transient ON (37%), primary-like (33%), or transient OFF (23%). When presented with sinusoidally amplitude modulated tones, most neurons had low-pass filter characteristics with cutoffs between 100 and 300 Hz modulation frequency. For comparison with the sinusoidally modulated sounds, we presented trains of tone pips in which the pulse duration and interstimulus interval were varied. The results of these experiments indicated that it is not the modulation frequency but rather the interstimulus interval that determines the low-pass filter characteristics of MSO neurons.

Responses to combinations of tones in the nuclei of the lateral lemniscus.

Combination-sensitive neurons integrate specific spectral and temporal elements in biologically important sounds, and they may underlie the analysis of biosonar and social vocalizations. Combination-sensitive neurons are found in the forebrain of a variety of vertebrates. In the mustached bat, they also occur in the central nucleus of the inferior colliculus (ICC). However, it is not known where combination-sensitive response properties emerge. To address this question, we used a two-tone paradigm to examine responses of single units to combination stimuli in a brainstem structure, the nuclei of the lateral lemniscus (NLL). We recorded and histologically localized 101 single units in the NLL. The majority (82%) of units had a single excitatory frequency tuning curve. Seven units had two separate excitatory frequency tuning curves but displayed no combinatorial interaction. Twelve units were combination-sensitive. Of these, three units were facilitated by the combination of two separate frequency bands and nine units were inhibited by combinatorial stimuli. The three facilitatory neurons had excitatory responses tuned to the second harmonic constant frequency (CF2, 57-60 kHz) component of the biosonar signal and were facilitated by a second signal within the first harmonic (Hl, 24-30 kHz) of the biosonar call. Most of the inhibitory interactions occurred between signals in the frequency bands associated with the frequency-modulated (FM) components of the biosonar call. The strongest combinatorial effects (facilitatory and inhibitory) were elicited by simultaneous onset of the two signals (i.e., 0 ms delay). All combination-sensitive units were in the intermediate nucleus of the NLL (INLL), which in bats is a hypertrophied structure that projects strongly to combination-sensitive neurons in the ICC. Thus, the combination-sensitive neurons in the INLL may impart their response properties onto ICC neurons. However, the small number of facilitatory combination-sensitive neurons in the NLL suggests that the majority of these combinatorial responses originate in the ICC.

Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices.

Auditory conditioning (associative learning) causes reorganization of the cochleotopic (frequency) maps of the primary auditory cortex (AI) and the inferior colliculus. Focal electric stimulation of the AI also evokes basically the same cortical and collicular reorganization as that caused by conditioning. Therefore, part of the neural mechanism for the plasticity of the central auditory system caused by conditioning can be explored by focal electric stimulation of the AI. The reorganization is due to shifts in best frequencies (BFs) together with shifts in frequency-tuning curves of single neurons. In the AI of the Mongolian gerbil (Meriones unguiculatus) and the posterior division of the AI of the mustached bat (Pteronotus parnellii), focal electric stimulation evokes BF shifts of cortical auditory neurons located within a 0.7-mm distance along the frequency axis. The amount and direction of BF shift differ depending on the relationship in BF between stimulated and recorded neurons, and between the gerbil and mustached bat. Comparison in BF shift between different mammalian species and between different cortical areas of a single species indicates that BF shift toward the BF of electrically stimulated cortical neurons (centripetal BF shift) is common in the AI, whereas BF shift away from the BF of electrically stimulated cortical neurons (centrifugal BF shift) is special. Therefore, we propose a hypothesis that reorganization, and accordingly organization, of cortical auditory areas caused by associative learning can be quite different between specialized and nonspecialized (ordinary) areas of the auditory cortex.

Spectral Integration in the Inferior Colliculus: Role of Glycinergic Inhibition in Response Facilitation

This study examined the contribution of glycinergic inhibition to the time-sensitive spectral integration performed by neurons in the inferior colliculus of the mustached bat (Pteronotus parnellii). These neurons are sometimes called combination-sensitive because they display facilitatory (or inhibitory) responses to the combination of distinct spectral elements in sonar or social vocalizations. Present in a wide range of vertebrates, their temporally and spectrally selective integration is thought to endow them with the ability to discriminate among social vocalizations or to analyze particular cues concerning sonar targets. The mechanisms that underlie these responses or the sites in the auditory system where they are created are not known. We examined combination-sensitive neurons that are facilitated by the presentation of two different harmonic elements of the bat's sonar call and echo. Responses of 24 single units were recorded before and during local application of strychnine, an antagonist of glycinergic inhibition. For each of the 24 units, strychnine application eliminated or greatly reduced temporally sensitive facilitation. There was no difference in this effect for neurons tuned to frequencies associated with the frequency-modulated or the constant-frequency sonar components. These results are unusual because glycine is considered to be an inhibitory neurotransmitter, but here it appears to be essential for the expression of combination-sensitive facilitation. The findings provide strong evidence that facilitatory combination-sensitive response properties present throughout the mustached bat's auditory midbrain, thalamus, and cortex originate through neural interactions in the inferior colliculus.

Topographical distribution of delay-tuned responses in the mustached bat inferior colliculus

In the mustached bat, delay-tuned neurons respond best to specific delays between the first harmonic frequency modulated (FM) component (FM1; 24–29 kHz) of the emitted biosonar pulse and a higher harmonic FM component in returning echoes (e.g. FM3, 72–89 kHz). These delay-tuned, combinatorial responses predominate in the inferior colliculus (IC) of the mustached bat. This study examined the topographical distribution of delay-tuned neurons in the 72–89 kHz frequency representation of the IC. We recorded and histologically localized 163 single units. Ninety units were facilitated and 41 were inhibited by the combination of two frequencies in the 24–29 kHz and 72–89 kHz ranges. The facilitatory responses were selective for delays up to 20 ms between the two signals. To determine if delay-tuned neurons were topographically organized, we plotted the dorsomedio–ventrolateral and caudo–rostral positions of each unit versus its best delay. Best delay was not correlated with either location. Response latency to best frequency tones was topographically organized, but was not correlated with best delay. This indicates that the latency axis in the IC is unrelated to the delay tuning of these combinatorial neurons. Because delay-tuned neurons are not topographically organized in the IC but are in the auditory cortex, our findings suggest that the creation and organization of delay-tuned neurons occur at different stages in the ascending auditory system.

Multiple combination-sensitive neurons in the auditory cortex of the mustached bat

The mustached bat, Pteronotus parnellii, emits biosonar pulses consisting of four constant-frequency (CF1–4) and four frequency-modulated (FM1–4) components. The FM–FM area of its auditory cortex consists of three subdivisions, containing either FM1–FM2, FM1–FM3 or FM1–FM4 combination-sensitive neurons. The FM–FM area also contains ‘multiple combination-sensitive’ neurons: FM1–FM2,3, FM1–FM3,4, FM1–FM2,4, and FM1–FM2,3,4 neurons. All FM–FM neurons are tuned to a time delay (echo delay) of FMn (n=2–4) from FM1. In the present study, we made the following four major findings. (1) Multiple combination-sensitive neurons show the strongest response to a combination of more than two signal elements. (2) Multiple combination-sensitive neurons are located in about 100 μm wide bands at the boundaries between two adjacent subdivisions of the FM–FM area. (3) Iso-best-delay contour lines across the three single combination-sensitive subdivisions are not interrupted by multiple combination-sensitive bands. (4) Each subdivision of the FM–FM area has frequency-vs.-frequency coordinates in terms of best FM1 and best FMn frequencies for facilitation, although such coordinates were not obtained with single tone bursts.

Consequences of outer hair cell damage for otoacoustic emissions and audio-vocal feedback in the mustached bat.

The cochlea of the mustached bat is adapted to process ultrasonic echolocation signals. To assess the involvement of active sound amplification by outer hair cells in high-frequency hearing and in audio-vocal interaction, selective hair cell damage was induced by the antibiotic Amikacin. Amikacin preferentially damaged the first row of outer hair cells in the basal cochlear turn. The cochlear regions coding for the second-harmonic constant-frequency component of the echolocation call (CF2) at 61 kHz and for frequencies between 75 and 100 kHz were the most affected. This was reflected in an increase of mechanical thresholds obtained by measuring distortion-product otoacoustic emissions. During initial periods of minor hair cell damage, when thresholds had deteriorated by less than 40 dB, a sharp, mechanical, cochlear resonance that is responsible for enhanced tuning to 61 kHz was still measurable as a stimulus-frequency otoacoustic emission and its frequency decreased by 350 Hz. The persistence of the resonance suggests that passive structures like the tectorial or basilar membrane are important for generation of the resonance. Behaviorally, the bats reacted to the change in cochlear micromechanics with a decrease of their CF2 frequency by 360 Hz. After larger hair cell damage, when the cochlear resonance had disappeared, the bats vocalized only sparsely and the CF2 frequency increased by up to 2 kHz, which may correspond to a state without audiovocal feedback. This indicates that audio-vocal feedback in the nondamaged animal works to lower the call frequency.

Spectral Integration in the Inferior Colliculus of the Mustached Bat

Acoustic behaviors including orientation and social communication depend on neural integration of information across the sound spectrum. In many species, spectral integration is performed by combination-sensitive neurons, responding best when distinct spectral elements in sounds are combined. These are generally considered a feature of information processing in the auditory forebrain. In the mustached bat's inferior colliculus (IC), they are common in frequency representations associated with sonar signals but have not been reported elsewhere in this bat's IC or the IC of other species. We examined the presence of combination-sensitive neurons in frequency representations of the mustached bat's IC not associated with biosonar. Seventy-five single-unit responses were recorded with the best frequencies in 10-23 or 32-47 kHz bands. Twenty-six displayed single excitatory tuning curves in one band with no additional responsiveness to a second signal in another band. The remaining 49 responded to sounds in both 10-23 and 32-47 kHz bands, but response types varied. Sounds in the higher band were usually excitatory, whereas sounds in the lower band either facilitated or inhibited responses to the higher frequency signal. Interactions were usually strongest when the higher and lower frequency stimuli were presented simultaneously, but the strength of interactions varied. Over one-third of the neurons formed a distinct subset; they responded most sensitively to bandpass noise, and all were combination sensitive. We suggest that these combination-sensitive interactions are activated by elements of mustached bat social vocalizations. If so, neuronal integration characterizing analysis of social vocalizations in many species occurs in the IC.

Shapes and level tolerances of frequency tuning curves in primary auditory cortex: quantitative measures and population codes.

The shape and level tolerance of the excitatory frequency/intensity tuning curves (eFTCs) of 160 cat primary auditory cortical (A1) neurons were investigated. Overall, A1 cells were characterized by tremendous variety in eFTC shapes and symmetries; eFTCs were U-shaped ( approximately 20%), V-shaped ( approximately 20%), lower-tail-upper-sharp ( approximately 15%), upper-tail-lower-sharp (<2%), slant-lower ( approximately 10%), slant-upper (<3%), multipeaked ( approximately 10%), and circumscribed ( approximately 20%). Quantitative analysis suggests that eFTC are best thought of as forming a continuum of shapes, rather than falling into discrete categories. A1 eFTCs tended to be more level tolerant than eFTCs from earlier stations in the ascending auditory system as inferred from other studies. While individual peaks of multipeaked eFTCs were similar to single peaked eFTCs, the overall eFTC of multipeaked neurons (spanning the range of all peaks) tended to have high-frequency tails. Measurements of shape and symmetry indicate that A1 eFTCs, on average, tended to have greater area on the low-frequency side of characteristic frequency (CF) than on the high-frequency side. A1 cells showed a relationship between CF and the inverse slope of low-frequency edges of eFTCs, but not for high-frequency edges. These data demonstrate that frequency tuning, particularly along the eFTC low-frequency border, sharpens along the lemniscal pathway to A1. The results are consistent with studies in mustached bats (Suga 1997) and support the idea that spectral decomposition along the ascending lemniscal pathway up to A1 is a general organizing principle of mammalian auditory systems. Altogether, these data suggest that A1 neurons' eFTCs are shaped by complex patterns of inhibition and excitation accumulating along the auditory pathways, implying that central rather than peripheral filtering properties are responsible for certain psychophysical phenomena.

Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats.

In the Jamaican mustached bat, Pteronotus parnellii parnellii, one of the subdivisions of the primary auditory cortex is disproportionately large and over-represents sound at approximately 61 kHz. This area, called the Doppler-shifted constant frequency (DSCF) processing area, consists of neurons extremely sharply tuned to a sound at approximately 61 kHz. We found that a focal activation of the DSCF area evokes highly specific corticofugal modulation in the inferior colliculus and medial geniculate body. Namely a focal activation of cortical DSCF neurons tuned to, say, 61. 2 kHz with 0.2-ms-long, 100-nA electric pulses drastically increases the excitatory responses of thalamic and collicular neurons tuned to 61.2 kHz without shifting their best frequencies (BFs). However, it decreases the excitatory responses of subcortical neurons tuned to frequencies slightly higher or lower than 61.2 kHz and shifts their BFs away from 61.2 kHz. The BF shifts are symmetrical and centrifugal around 61.2 kHz. These corticofugal effects are larger on thalamic neurons than on collicular neurons. The cortical electrical stimulation sharpens the frequency-tuning curves of subcortical neurons. These corticofugal effects named "egocentric selection" last </=2.5 h after the cessation of a 7-min-long cortical electrical stimulation. In the mustached bat, corticofugal modulation serves to increase the contrast in neural representation of sound at approximately 61 kHz, which is an important component of an echo bearing velocity information. It is also most likely that the corticofugal system plays an important role in plasticity of the central auditory system. Another subdivision of the auditory cortex of the mustached bat is called the FM-FM area. This area consists of delay-tuned combination-sensitive neurons, called FM-FM neurons, and has the echo-delay axis for the systematic representation of target distances. A focal electric stimulation of the FM-FM area evokes changes in the responses of collicular and thalamic FM-FM neurons. These changes are basically the same as those described in the present paper. Therefore corticofugal modulation takes place for frequency domain analysis in exactly the same way as it does in time domain analysis.

The tympanic membrane: Highly developed smooth muscle arrays in the annulus fibrosus of mustached bats

The annulus fibrosus tympanicus is the thickened peripheral rim of the pars tensa of the tympanic membrane. It is an area into which the connective tissue matrix of the membrane extends to attach to the tympanic bone (ring). Light microscopy, SEM, TEM and confocal microscopy were used to study the area in mustached bats Pteronotus p. parnellii, P. p. portoricensis and P. quadridens. In cross sections of the annulus morphologically distinct apical and basal or myovascular zones could be recognized. The apical zone had a collagenous matrix that was continuous with the pars tensa. The myovascular zone contained an extensive network of thin walled endothelial tubes and a well-developed array of radially arranged smooth muscle cells that filled the interval between the vessels. The muscle tissue occupied the interval between the densely collagenous "apical zone" and the bony tympanic ring and was closely associated with bundles of unmyelinated nerve fibers. The structure and arrangement of the tissue suggests a highly developed specialization for the tonic control of tension of the pars tensa and a system that potentially regulates sound transmission to the middle and inner ear.

Auditory responses from the frontal cortex in the mustached bat, Pteronotus parnellii.

Response properties of neurons in an auditory field in the frontal cortex of the mustached bat, Pteronotus parnellii, have not been studied before. We recorded neural responses to constant frequency (CF) stimuli from the frontal auditory field in awake animals. The majority (75%) of neurons in this area responded well and often exhibited low thresholds to CF stimuli. Most CF-responsive neurons exhibited sharp tuning with values of > 180 for Q10db, a quality factor expressing the sharpness of tuning at 10dB above threshold. Neurons at 13 recording sites exhibited combination sensitivity in that their responses were facilitated by presenting combinations of either CF1/CF2 and/or CF1/CF3 components of the mustached bat's echolocation signal. Unlike the typical on-responses to a 30 ms tone, observed in the mustached bat's auditory cortex and at subcortical levels, many frontal auditory neurons exhibited loosely time locked firing patterns that lasted for > 100 ms.

The tympanic membrane: Highly developed smooth muscle arrays in the annulus fibrosus of mustached bats

The tympanic membrane: Highly developed smooth muscle arrays in the annulus fibrosus of mustached bats

Anatomical and functional imaging of the auditory cortex in awake mustached bats using magnetic resonance technology

The auditory cortex of mustached bats, Pteronotus parnellii, has been studied extensively using neuroanatomical tract-tracing and electrophysiological techniques to elucidate the functional organization and neural mechanisms important for auditory processing. While these techniques have identified several cortical maps involved in processing auditory information, there has been no direct observation of the dynamics of simultaneous activation of several discrete areas. We applied magnetic resonance (MR) imaging techniques for visualizing brain structures in awake bats using a 7-Tesla magnet system; we also investigated functional MR imaging by measuring changes in stimulus-correlated blood oxygenation levels to detect cortical areas exhibiting evoked neural activity. High resolution (100 μm) anatomical images were successfully acquired without any motion artifacts. It was possible to reconstruct the whole brain image and analyze brain surface structures with three dimensional (3D) MR imaging data. These data provide detailed morphometric measurements that will allow localization of stimulus specific neural activity patterns using modified functional magnetic-resonance-imaging (fMRI) protocols. Motion artifacts is the primary disadvantage of using awake bats; our study shows that fMRI of a bat's brain is feasible and may prove to be an important advancement for a further understanding of auditory processing in this species. Themes: Sensory systems, Neural basis of behavior. Topics: Auditory systems: central anatomy, Auditory systems: central physiology, Neuroethology, Neural plasticity.

Frequency organization and responses to complex sounds in the medial geniculate body of the mustached bat.

The auditory cortex of the mustached bat (Pteronotus parnellii) displays some of the most highly developed physiological and organizational features described in mammalian auditory cortex. This study examines response properties and organization in the medial geniculate body (MGB) that may contribute to these features of auditory cortex. About 25% of 427 auditory responses had simple frequency tuning with single excitatory tuning curves. The remainder displayed more complex frequency tuning using two-tone or noise stimuli. Most of these were combination-sensitive, responsive to combinations of different frequency bands within sonar or social vocalizations. They included FM-FM neurons, responsive to different harmonic elements of the frequency modulated (FM) sweep in the sonar signal, and H1-CF neurons, responsive to combinations of the bat's first sonar harmonic (H1) and a higher harmonic of the constant frequency (CF) sonar signal. Most combination-sensitive neurons (86%) showed facilitatory interactions. Neurons tuned to frequencies outside the biosonar range also displayed combination-sensitive responses, perhaps related to analyses of social vocalizations. Complex spectral responses were distributed throughout dorsal and ventral divisions of the MGB, forming a major feature of this bat's analysis of complex sounds. The auditory sector of the thalamic reticular nucleus also was dominated by complex spectral responses to sounds. The ventral division was organized tonotopically, based on best frequencies of singly tuned neurons and higher best frequencies of combination-sensitive neurons. Best frequencies were lowest ventrolaterally, increasing dorsally and then ventromedially. However, representations of frequencies associated with higher harmonics of the FM sonar signal were reduced greatly. Frequency organization in the dorsal division was not tonotopic; within the middle one-third of MGB, combination-sensitive responses to second and third harmonic CF sonar signals (60-63 and 90-94 kHz) occurred in adjacent regions. In the rostral one-third, combination-sensitive responses to second, third, and fourth harmonic FM frequency bands predominated. These FM-FM neurons, thought to be selective for delay between an emitted pulse and echo, showed some organization of delay selectivity. The organization of frequency sensitivity in the MGB suggests a major rewiring of the output of the central nucleus of the inferior colliculus, by which collicular neurons tuned to the bat's FM sonar signals mostly project to the dorsal, not the ventral, division. Because physiological differences between collicular and MGB neurons are minor, a major role of the tecto-thalamic projection in the mustached bat may be the reorganization of responses to provide for cortical representations of sonar target features.

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.