Auditory Cortex Of Mustached Bat Research Articles

A three-dimensional digital neurological atlas of the mustached bat (Pteronotus parnellii)

Substantial knowledge of auditory processing within mammalian nervous systems emerged from neurophysiological studies of the mustached bat (Pteronotus parnellii). This highly social and vocal species retrieves precise information about the velocity and range of its targets through echolocation. Such high acoustic processing demands were likely the evolutionary pressures driving the over-development at peripheral (cochlea), metencephalic (cochlear nucleus), mesencephalic (inferior colliculus), diencephalic (medial geniculate body of the thalamus), and telencephalic (auditory cortex) auditory processing levels in this species. Auditory researchers stand to benefit from a three dimensional brain atlas of this species, due to its considerable contribution to auditory neuroscience. Our MRI-based atlas was generated from 2 sets of image data of an ex-vivo male mustached bat's brain: a detailed 3D-T2-weighted-RARE scan [(59 × 63 x 85) μm3] and track density images based on super resolution diffusion tensor images [(78) μm3] reconstructed from a set of low resolution diffusion weighted images using Super-Resolution-Reconstruction (SRR). By surface-rendering these delineations and extrapolating from cortical landmarks and data from previous studies, we generated overlays that estimate the locations of classic functional subregions within mustached bat auditory cortex. This atlas is freely available from our website and can simplify future electrophysiological, microinjection, and neuroimaging studies in this and related species.

Acuity in ranging based on delay-tuned combination-sensitive neurons in the auditory cortex of mustached bats

A 1.0-ms echo delay from an emitted bio-sonar pulse at 25 °C corresponds to a 17.3-cm target distance. In the auditory cortex of the mustached bat, Pteronotus parnellii, neurons tuned to a specific delay (best delay) of an echo from an emitted pulse are clustered in the FF, dorsal fringe and ventral fringe areas. (“FF” stands for the frequency-modulated components of a pulse and its echo.) Those delay-tuned neurons are systematically arranged in the FF area according to their best delays and form a 18-ms-long delay axis. Using the neurophysiological data, the theoretical acuity at a 75% correct level was computed as just-noticeable changes in (a) the location of maximally responding delay-tuned neurons, (b) the location of the center of all responses in the FF area, and (c) the weighted sum of responses of all delay-tuned neurons. The acuity is range-dependent: the shorter the target range, the higher the acuity is. The just-noticeable changes in target range are 7.57–46.2, 0.50–2.32 and 0.22–2.53 mm at the target ranges of up to 140 cm for (a), (b) and (c), respectively. When the dorsal and ventral fringe areas are included in the computation, the just-noticeable changes become smaller than those in the FF area alone. Those acuities computed are comparable to certain behavioral acuities.

Differences in velocity-information processing between two areas in the auditory cortex of mustached bats

The bio-sonar pulse of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics of constant frequency (CF1-4) and frequency-modulated (FM1-4) components. The CF and FM components carry velocity and distance information, respectively. In the auditory cortex of mustached bats, the CC (“C” stands for constant frequency) and DIF (dorsal intrafossa) areas consist of CF/CF neurons tuned to a combination of pulse CF1 and echo CFn (n = 2 or 3). They show facilitative responses to pulse-echo stimuli with specific frequency differences, corresponding to Doppler shifts. Their facilitative responses are sharply tuned to a specific relative target velocity (best velocity). Compared with CC neurons, DIF neurons are tuned to higher velocities and to larger CF1 amplitudes, and adapt faster to repetitive pulse-echo stimuli. The great majority of CC neurons are suited for the processing of velocity information during cruising and target-directed flight, whereas the majority of DIF neurons are suited for the processing of velocity information when the bat is emitting loud pulses at low repetition rates during cruising flight. CC and DIF neurons are broadly tuned to 0–2-ms echo delays and not suited for ranging.

Social Calls Exhibit a Distributed Consensus Map in the Auditory Cortex of Mustached Bats

Social Calls Exhibit a Distributed Consensus Map in the Auditory Cortex of Mustached Bats

Neural Coding of Call Pitch and Syllable Type in the Auditory Cortex of Mustached Bats

Neural Coding of Call Pitch and Syllable Type in the Auditory Cortex of Mustached Bats

Right–left asymmetry in the cortical processing of sounds for social communication vs. navigation in mustached bats

In the Doppler-shifted constant frequency processing area in the primary auditory cortex of mustached bats, Pteronotus parnellii, neurons respond to both social calls and to echolocation signals. This multifunctional nature of cortical neurons creates a paradox for simultaneous processing of two behaviorally distinct categories of sound. To test the possibility of a stimulus-specific hemispheric bias, single-unit responses were obtained to both types of sounds, calls and pulse-echo tone pairs, from the right and left auditory cortex. Neurons on the left exhibited only slightly higher peak response magnitudes for their respective best calls, but they showed a significantly higher sensitivity (lower response thresholds) to calls than neurons on the right. On average, call-to-tone response ratios were significantly higher for neurons on the left than for those on the right. Neurons on the right responded significantly more strongly to pulse-echo tone pairs than those on the left. Overall, neurons in males responded to pulse-echo tone pairs with a much higher spike count compared to females, but this difference was less pronounced for calls. Multidimensional scaling of call responses yielded a segregated representation of call types only on the left. These data establish for the first time, a behaviorally directed right-left asymmetry at the level of single cortical neurons. It is proposed that a lateralized cortex emerges from multiparametric integration (e.g. combination-sensitivity) within a neuron and inhibitory interactions between neurons that come into play during the processing of complex sounds.

DSCF neurons within the primary auditory cortex of the mustached bat process frequency modulations present within social calls.

Neurons in the Doppler-shifted constant frequency processing (DSCF) area in the primary auditory cortex of mustached bats, Pteronotus parnellii, are multifunctional, responding both to echolocation and communication sounds. Simultaneous presentation of a DSCF neuron's best low and high frequencies (BF(low) and BF(high), respectively) facilitates its response. BF(low) corresponds to a frequency in the frequency-modulated (FM) component of the first harmonic in the echolocation pulse, and BF(high) corresponds to the constant frequency (CF) component in the second harmonic of the echo. We systematically varied the slopes, bandwidths, and central frequencies of FMs traversing the BF(high) region to arrive at the "best FM" for single DSCF neurons. We report that nearly half (46%) of DSCF neurons preferred linear FMs to CFs and average response magnitude to FMs was not significantly less (P = 0.08) than that to CFs at BF(high) when each test stimulus was paired with a CF at BF(low). For linear FMs ranging in slope from 0.04 to 4.0 kHz/ms and in bandwidth from 0.44 to 7.88 kHz, the majority of DSCF neurons preferred upward (55%) to downward (21%) FMs. Central frequencies of the best FMs were typically close to but did not always match a neuron's BF(high). Neurons exhibited combination-sensitivity to "call fragments" (calls that were band-pass filtered in the BF(high) region) paired with their BF(low). Our data show a close match between the modulation direction of a neuron's best FM and that of its preferred call fragment. These response properties show that DSCF neurons extract multiple parameters of FMs and are specialized for processing both FMs for communication and CFs for echolocation.

Connections of functional areas in the mustached bat's auditory cortex with the auditory thalamus

The auditory thalamus is the major target of the inferior colliculus and connects in turn with the auditory cortex. In the mustached bat, biosonar information is represented according to frequency in the central nucleus of the inferior colliculus (ICc) but according to response type in the cortex. In addition, the cortex has multiple areas with neurons of similar response type compared to the single tonotopic representation in the ICc. To investigate whether these transformations occur at the level of the thalamus, we injected anatomical tracers into physiologically defined locations in the mustached bat's auditory cortex. Injections in areas used for target ranging labeled contiguous regions of the auditory thalamus rather than separate patches corresponding to regions that respond to the different harmonic frequencies used for ranging. Injections in the two largest ranging areas produced labeling in separate locations. These results indicate that the thalamus is organized according to response type rather than frequency and that multiple mappings of response types exist. Injections in areas used for target detection labeled thalamic regions that were largely separate from those that interconnect with ranging areas. However, injections in an area used for determining target velocity overlapped with the areas connected to ranging areas and areas involved in target detection. Thus, separation by functional type and multiplication of areas with similar response type occurs by the thalamic level, but connections with the cortex segregate the functional types more completely than occurs in the thalamus.

Is humanlike cytoarchitectural asymmetry present in another species with complex social vocalization? A stereologic analysis of mustached bat auditory cortex

Considerable evidence suggests that left hemispheric lateralization for language comprehension in humans is associated with cortical microstructural asymmetries. However, despite the fact that left hemispheric dominance for the analysis of species-specific social vocalizations has been reported in several other species, little is known concerning microstructural asymmetries in auditory cortex of nonhumans. To test whether such neuroanatomical lateralization characterizes another species with complex social vocalizations, we performed stereologic analyses of Nissl-stained cells in layer III of area DSCF in mustached bats ( Pteronotus parnellii). Area DSCF was selected because it contains neurons which are sensitive to several temporal features of conspecific vocalizations. Primary visual cortex (V1) was also studied as a comparative reference. We measured neuron densities, glial densities, and neuronal volumes in both hemispheres of 10 adult male bats. Results indicate that these variables are not significantly lateralized in area DSCF or V1. Additionally, magnopyramidal cells (i.e., the largest 10% of neurons from both hemispheres) were not asymmetric in their frequency of distribution at the population level. Although several individual bats had asymmetric neuron distributions, consistent hemispheric bias was not evident. Absence of population-level microstructural asymmetry in area DSCF of mustached bats suggests alternative evolutionary scenarios including: (1) microstructural lateralization of auditory cortical circuitry may be a unique adaptation for human language, and (2) the specialized biosonar function of mustached bat auditory cortex may require symmetrical cytoarchitectural structure. Resolution of these alternatives will require further data on the microstructure of auditory cortex in species with lateralized perception of acoustic social communication.

Neurodynamics for auditory stream segregation: tracking sounds in the mustached bat's natural environment

During navigation and the search phase of foraging, mustached bats emit ∼25 ms long echolocation pulses (at 10–40 Hz) that contain multiple harmonics of a constant frequency (CF) component followed by a short (3 ms) downward frequency modulation. In the context of auditory stream segregation, therefore, bats may either perceive a coherent pulse–echo sequence (PEPE…), or segregated pulse and echo streams (P–P–P… and E–E–E…). To identify the neural mechanisms for stream segregation in bats, we developed a simple yet realistic neural network model with seven layers and 420 nodes. Our model required recurrent and lateral inhibition to enable output nodes in the network to ‘latch-on’ to a single tone (corresponding to a CF component in either the pulse or echo), i.e., exhibit differential suppression by the alternating two tones presented at a high rate (>10 Hz). To test the applicability of our model to echolocation, we obtained neurophysiological data from the primary auditory cortex of awake mustached bats. Event-related potentials reliably reproduced the latching behaviour observed at output nodes in the network. Pulse as well as nontarget (clutter) echo CFs facilitated this latching. Individual single unit responses were erratic, but when summed over several recording sites, they also exhibited reliable latching behaviour even at 40 Hz. On the basis of these findings, we propose that a neural correlate of auditory stream segregation is present within localized synaptic activity in the mustached bat's auditory cortex and this mechanism may enhance the perception of echolocation sounds in the natural environment.

Neurodynamics for auditory stream segregation: tracking sounds in the mustached bat's natural environment

During navigation and the search phase of foraging, mustached bats emit ∼25 ms long echolocation pulses (at 10–40 Hz) that contain multiple harmonics of a constant frequency (CF) component followed by a short (3 ms) downward frequency modulation. In the context of auditory stream segregation, therefore, bats may either perceive a coherent pulse–echo sequence (PEPE…), or segregated pulse and echo streams (P–P–P… and E–E–E…). To identify the neural mechanisms for stream segregation in bats, we developed a simple yet realistic neural network model with seven layers and 420 nodes. Our model required recurrent and lateral inhibition to enable output nodes in the network to ‘latch-on’ to a single tone (corresponding to a CF component in either the pulse or echo), i.e., exhibit differential suppression by the alternating two tones presented at a high rate (>10 Hz). To test the applicability of our model to echolocation, we obtained neurophysiological data from the primary auditory cortex of awake mustached bats. Event-related potentials reliably reproduced the latching behaviour observed at output nodes in the network. Pulse as well as nontarget (clutter) echo CFs facilitated this latching. Individual single unit responses were erratic, but when summed over several recording sites, they also exhibited reliable latching behaviour even at 40 Hz. On the basis of these findings, we propose that a neural correlate of auditory stream segregation is present within localized synaptic activity in the mustached bat's auditory cortex and this mechanism may enhance the perception of echolocation sounds in the natural environment.

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.

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.

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.

Connections among functional areas in the mustached bat auditory cortex

Connections among functional areas in the mustached bat's auditory cortex were examined by placing anatomical tracers in physiologically defined locations. We identified at least two and probably three channels connecting the various areas. One channel is formed by interconnections among areas containing neurons sensitive to frequency-modulated components (FMs) of the pulse and echo. These neurons are tuned to echo delay, a cue for target range, and thus define a ranging channel. An additional one or two channels are formed by interconnections among areas that contain neurons sensitive to the constant frequency components (CFs) of echoes. These neurons are of two main types: either sensitive to CFs of both pulse and echo (CF/CF neurons) or sensitive to a pulse FM and echo CF (FM-CF neurons). There was only a weak connection between the largest area of each type, suggesting they lie in different channels. Connections among areas in the ranging channel and echo CF-sensitive channel(s) were weak. Thus, the interconnections among functional areas in the mustached bat's auditory cortex define parallel channels for processing different types of biosonar information. Most corticocortical connections were patchy, in a manner suggestive of a columnar organization. The average width of the patches was approximately 360 μm. Based on the sizes of the functional areas, we estimate the auditory cortex contains a total of approximately 150 columns. Individual areas contain from as many as approximately 20 to as few as 1–4 columns. Each area had abundant projections outside of the auditory cortex. Connections within the cortex included the frontal, anterior cingulate, retrosplenial and perirhinal cortices, and the claustrum. Subcortical targets included the amygdyla, auditory thalamus, pons, pretectum, superior and inferior colliculi, and central gray. Projections within the cortex were of modest strength compared with several of the subcortical projections. Thus, the auditory areas themselves are the primary source of cortically processed biosonar information to the rest of the brain. J. Comp. Neurol. 391:366–396, 1998. © 1998 Wiley-Liss, Inc.

Connections among functional areas in the mustached bat auditory cortex

Connections among functional areas in the mustached bat's auditory cortex were examined by placing anatomical tracers in physiologically defined locations. We identified at least two and probably three channels connecting the various areas. One channel is formed by interconnections among areas containing neurons sensitive to frequency-modulated components (FMs) of the pulse and echo. These neurons are tuned to echo delay, a cue for target range, and thus define a ranging channel. An additional one or two channels are formed by interconnections among areas that contain neurons sensitive to the constant frequency components (CFs) of echoes. These neurons are of two main types: either sensitive to CFs of both pulse and echo (CF/CF neurons) or sensitive to a pulse FM and echo CF (FM-CF neurons). There was only a weak connection between the largest area of each type, suggesting they lie in different channels. Connections among areas in the ranging channel and echo CF-sensitive channel(s) were weak. Thus, the interconnections among functional areas in the mustached bat's auditory cortex define parallel channels for processing different types of biosonar information. Most corticocortical connections were patchy, in a manner suggestive of a columnar organization. The average width of the patches was approximately 360 microm. Based on the sizes of the functional areas, we estimate the auditory cortex contains a total of approximately 150 columns. Individual areas contain from as many as approximately 20 to as few as 1-4 columns. Each area had abundant projections outside of the auditory cortex. Connections within the cortex included the frontal, anterior cingulate, retrosplenial and perirhinal cortices, and the claustrum. Subcortical targets included the amygdyla, auditory thalamus, pons, pretectum, superior and inferior colliculi, and central gray. Projections within the cortex were of modest strength compared with several of the subcortical projections. Thus, the auditory areas themselves are the primary source of cortically processed biosonar information to the rest of the brain.

Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

AILDD1 AC'1 The responses of neurons in the mustached bat's auditory cortex are specialized to extract particular information from biosonar signals. For this study, we mapped response properties across entire hemispheres in several animals. These experiments enabled us to construct a standard map that aided in determining the connections among the areas, as described subsequently. The mapping also yielded quantitative data regarding the relative sizes of areas and the proportion of cortex devoted to different response types. We identified six response types that were distributed in 11 areas. Eight areas, comprising two-thirds of the auditory cortex, contained neurons sensitive to particular components in biosonar signals. Most were facilitated by combinations of frequency modulated and constant frequency biosonar signal components (FMs and CFs, respectively). There were three major types of combination-sensitive neurons: FM-FM, CF/CF, and FM-CF. Each type of combination sensitivity occurred in multiple areas. The largest proportion were FM-FM neurons (approximately 30% of all neurons in auditory cortex), followed by FM1-CF2 (approximately 23%) and CF/CF (approximately 11%). In the other three areas comprising approximately one-third of the auditory cortex, most neurons responded well to frequencies not contained in biosonar signals.

Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

Connections among functional areas in the mustached bat auditory cortex

Connections among functional areas in the mustached bat auditory cortex

Distribution of response types across entire hemispheres of the mustached bat's auditory cortex

The responses of neurons in the mustached bat's auditory cortex are specialized to extract particular information from biosonar signals. For this study, we mapped response properties across entire hemispheres in several animals. These experiments enabled us to construct a standard map that aided in determining the connections among the areas, as described subsequently. The mapping also yielded quantitative data regarding the relative sizes of areas and the proportion of cortex devoted to different response types. We identified six response types that were distributed in 11 areas. Eight areas, comprising two-thirds of the auditory cortex, contained neurons sensitive to particular components in biosonar signals. Most were facilitated by combinations of frequency modulated and constant frequency biosonar signal components (FMs and CFs, respectively). There were three major types of combination-sensitive neurons: FM-FM, CF/CF, and FM-CF. Each type of combination sensitivity occurred in multiple areas. The largest proportion were FM-FM neurons (approximately 30% of all neurons in auditory cortex), followed by FM1-CF2 (approximately 23%) and CF/CF (approximately 11%). In the other three areas comprising approximately one-third of the auditory cortex, most neurons responded well to frequencies not contained in biosonar signals. J. Comp. Neurol. 391:353–365, 1998. © 1998 Wiley-Liss, Inc.