A model of anuran auditory periphery reveals frequency-dependent adaptation to be a contributing mechanism for two-tone suppression and amplitude modulation coding.

Anuran auditory nerve fibers (ANF) tuned to low frequencies display unusual frequency-dependent adaptation which results in a more phasic response to signals above best frequency (BF) and a more tonic response to signals below. A network model of the first two layers of the anuran auditory system was used to test the contribution of this dynamic peripheral adaptation on two-tone suppression and amplitude modulation (AM) tuning. The model included a peripheral sandwich component, leaky-integrate-and-fire cells and adaptation was implemented by means of a non-linear increase in threshold weighted by the signal frequency. The results of simulations showed that frequency-dependent adaptation was both necessary and sufficient to produce high-frequency-side two-tone suppression for the ANF and cells of the dorsal medullary nucleus (DMN). It seems likely that both suppression and this dynamic adaptation share a common mechanism. The response of ANFs to AM signals was influenced by adaptation and carrier frequency. Vector strength synchronization to an AM signal improved with increased adaptation. The spike rate response to a carrier at BF was the expected flat function with AM rate. However, for non-BF carrier frequencies the response showed a weak band-pass pattern due to the influence of signal sidebands and adaptation. The DMN received inputs from three ANFs and when the frequency tuning of inputs was near the carrier, then the rate response was a low-pass or all-pass shape. When most of the inputs were biased above or below the carrier, then band-pass responses were observed. Frequency-dependent adaptation enhanced the band-pass tuning for AM rate, particularly when the response of the inputs was predominantly phasic for a given carrier. Different combinations of inputs can therefore bias a DMN cell to be especially well suited to detect specific ranges of AM rates for a particular carrier frequency. Such selection of inputs would clearly be advantageous to the frog in recognizing distinct spectral and temporal parameters in communication calls.

Echo delay versus spectral cues for temporal hyperacuity in the big brown bat, Eptesicus fuscus.

Big brown bats can discriminate between echoes that alternate in delay (jitter) by as little as 10-15 ns and echoes that are stationary in delay. This delay hyperacuity seems so extreme that it has been rejected in favor of an explanation in terms of artifacts in echoes, most likely spectral in nature, that presumably are correlated with delay. Using different combinations of digital, analog, and cable delays, we dissociated the overall delay of jittering echoes from the size of the analog component of delay, which alone is presumed to determine the strength of the apparatus artifact. The bats' performance remains invariant with respect to the overall delay of the jittering echoes, not with respect to the amount of analog delay. This result is not consistent with the possible use of delay-related artifacts produced by the analog delay devices. Moreover, both electronic and acoustic measurements disclose no spectral cues or impedance-mismatch reflections in delayed signals, just time-delays. The absence of artifacts from the apparatus and the failure of overlap and interference from reverberation to account for the 10-ns result means that closing the gap between the level of temporal accuracy plausibly explained from physiology and the level observed in behavior may require a better understanding of the physiology.

Role of intrinsic conductances underlying responses to transients in octopus cells of the cochlear nucleus.

Recognition of acoustic patterns in natural sounds depends on the transmission of temporal information. Octopus cells of the mammalian ventral cochlear nucleus form a pathway that encodes the timing of firing of groups of auditory nerve fibers with exceptional precision. Whole-cell patch recordings from octopus cells were used to examine how the brevity and precision of firing are shaped by intrinsic conductances. Octopus cells responded to steps of current with small, rapid voltage changes. Input resistances and membrane time constants averaged 2.4 MOmega and 210 microseconds, respectively (n = 15). As a result of the low input resistances of octopus cells, action potential initiation required currents of at least 2 nA for their generation and never occurred repetitively. Backpropagated action potentials recorded at the soma were small (10-30 mV), brief (0.24-0.54 msec), and tetrodotoxin-sensitive. The low input resistance arose in part from an inwardly rectifying mixed cationic conductance blocked by cesium and potassium conductances blocked by 4-aminopyridine (4-AP). Conductances blocked by 4-AP also contributed to the repolarization of the action potentials and suppressed the generation of calcium spikes. In the face of the high membrane conductance of octopus cells, sodium and calcium conductances amplified depolarizations produced by intracellular current injection over a time course similar to that of EPSPs. We suggest that this transient amplification works in concert with the shunting influence of potassium and mixed cationic conductances to enhance the encoding of the onset of synchronous auditory nerve fiber activity.

Golgi cells in the superficial granule cell domain overlying the ventral cochlear nucleus: morphology and electrophysiology in slices.

Golgi cells are poised to integrate multimodal influences by participating in circuits involving granule cells in the cochlear nuclei. To understand their physiological role, intracellular recordings were made from anatomically identified Golgi cells in slices of the cochlear nuclei from mice. Cell bodies, dendrites, and terminals for all seven labeled cells were restricted to the narrow plane of the superficial granule cell domain over the ventral cochlear nucleus. The axonal arborization was the most striking feature of all Golgi cells; a dense plexus of terminals covered an area 200-400 microm in diameter in the vicinity of the cell body and dendrites. Axonal beads often surrounded granule cell bodies, indicating that granule cells are probable targets. Cells had input resistances up to 130 M omega and fired regular, overshooting action potentials. Golgi cells probably receive auditory nerve input, because shocks to the cut end of the auditory nerve excited Golgi cells with excitatory postsynaptic potentials (EPSPs). The latency of EPSPs shortened to a minimum and the amplitude of EPSPs grew in several steps as the strength of shocks was increased. The minimum latency of EPSPs in Golgi cells was on average 1.3 milliseconds, 0.6 milliseconds longer than the minimum latencies of EPSPs in nearby octopus and T stellate cells. The long latency raises the possibility that Golgi cells receive input from slowly conducting, unmyelinated auditory nerve fibers. Golgi cells are also excited by interneurons with N-methyl-D-aspartate receptors, probably granule cells, because repetitive shocks and single shocks in the absence of extracellular Mg2+ evoked late EPSPs that were reversibly blocked by DL-2-amino-5-phosphono-valeric acid.

Echo-delay resolution in sonar images of the big brown bat, Eptesicus fuscus.

Echolocating big brown bats (Eptesicus fuscus) broadcast ultrasonic frequency-modulated (FM) biosonar sounds (20-100 kHz frequencies; 10-50 microseconds periods) and perceive target range from echo delay. Knowing the acuity for delay resolution is essential to understand how bats process echoes because they perceive target shape and texture from the delay separation of multiple reflections. Bats can separately perceive the delays of two concurrent electronically generated echoes arriving as little as 2 microseconds apart, thus resolving reflecting points as close together as 0.3 mm in range (two-point threshold). This two-point resolution is roughly five times smaller than the shortest periods in the bat's sounds. Because the bat's broadcasts are 2,000-4,500 microseconds long, the echoes themselves overlap and interfere with each other, to merge together into a single sound whose spectrum is shaped by their mutual interference depending on the size of the time separation. To separately perceive the delays of overlapping echoes, the bat has to recover information about their very small delay separation that was transferred into the spectrum when the two echoes interfered with each other, thus explicitly reconstructing the range profile of targets from the echo spectrum. However, the bat's 2-microseconds resolution limit is so short that the available spectral cues are extremely limited. Resolution of delay seems overly sharp just for interception of flying insects, which suggests that the bat's biosonar images are of higher quality to suit a wider variety of orientation tasks, and that biosonar echo processing is correspondingly more sophisticated than has been suspected.

Frequency tuning, latencies, and responses to frequency-modulated sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus.

Neurons in the inferior colliculus (IC) of the awake big brown bat, Eptesicus fuscus, were examined for joint frequency and latency response properties which could register the timing of the bat's frequency-modulated (FM) biosonar echoes. Best frequencies (BFs) range from 10 kHz to 100 kHz with 50% tuning widths mostly from 1 kHz to 8 kHz. Neurons respond with one discharge per 2-ms tone burst or FM stimulus at a characteristic latency in the range of 3-45 ms, with latency variability (SD) of 50 microseconds to 4-6 ms or more. BF distribution is related to biosonar signal structure. As observed previously, on a linear frequency scale BFs appear biased to lower frequencies, with 20-40 kHz overrepresented. However, on a hyperbolic frequency (linear period) scale BFs appear more uniformly distributed, with little overrepresentation. The cumulative proportion of BFs in FM1 and FM2 bands reconstructs a scaled version of the spectrogram of FM broadcasts. Correcting FM latencies for absolute BF latencies and BF time-in-sweep reveals a subset of IC cells which respond dynamically to the timing of their BFs in FM sweeps. Behaviorally, Eptesicus perceives echo delay and phase with microsecond or even submicrosecond accuracy and resolution, but even with use of phase-locked FM and tone-burst stimuli the cell-by-cell precision of IC time-frequency registration seems inadequate by itself to account for the temporal acuity exhibited by the bat.

Synaptic inputs to stellate cells in the ventral cochlear nucleus.

Auditory information is carried from the cochlear nuclei to the inferior colliculi through six parallel ascending pathways, one of which is through stellate cells of the ventral cochlear nuclei (VCN) through the trapezoid body. To characterize and identify the synaptic influences on T stellate cells, intracellular recordings were made from anatomically identified stellate cells in parasagittal slices of murine cochlear nuclei. Shocks to the auditory nerve consistently evoked five types of synaptic responses in T stellate cells, which reflect sources intrinsic to the cochlear nuclear complex. 1) Monosynaptic excitatory postsynaptic potentials (EPSPs) that were blocked by 6,7-dinitroquinoxaline-2,3-dione (DNQX), an antagonist of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors, probably reflected activation by auditory nerve fibers. Electrophysiological estimates indicate that about five auditory nerve fibers converge on one T stellate cell. 2) Disynaptic, glycinergic inhibitory postsynaptic potentials (IPSPs) arise through inhibitory interneurons in the VCN or in the dorsal cochlear nucleus (DCN). 3) Slow depolarizations, the source of which has not been identified, that lasted between 0.2 and 1 s and were blocked by -2-amino-5-phosphonovaleric acid (APV), the N-methyl-D-aspartate (NMDA) receptor antagonist. 4) Rapid, late glutamatergic EPSPs are polysynaptic and may arise from other T stellate cells. 5) Trains of late glycinergic IPSPs after single or repetitive shocks match the responses of D stellate cells, showing that D stellate cells are one source of glycinergic inhibition to T stellate cells. The source of late, polysynaptic EPSPs and IPSPs was assessed electrophysiologically and pharmacologically. Late synaptic responses in T stellate cells were enhanced by repetitive stimulation, indicating that the interneurons from which they arose should fire trains of action potentials in responses to trains of shocks. Late EPSPs and late IPSPs were blocked by APV and enhanced by the removal of Mg2+, indicating that the interneurons were driven at least in part through NMDA receptors. Bicuculline, a gamma-aminobutyric acid-A (GABAA) receptor antagonist, enhanced the late PSPs, indicating that GABAergic inhibition suppresses both the glycinergic interneurons responsible for the trains of IPSPs in T-stellate cells and the interneuron responsible for late EPSPs in T stellate cells. The glycinergic interneurons that mediate the series of IPSPs are intrinsic to the ventral cochlear nucleus because long series of IPSPs were recorded from T stellate cells in slices in which the DCN was removed. These experiments indicate that T stellate cells are a potential source of late EPSPs and that D stellate cells are a potential source for trains of late IPSPs.

Sound source elevation and external ear cues influence the discrimination of spectral notches by the big brown bat, Eptesicus fuscus.

Measurements of external ear transfer functions in the echolocating bat Eptesicus fuscus have revealed a prominent spectral notch that decreases in center frequency (50 to 30-35 kHz) as elevation decreases [Wotton et al., J. Acoust. Soc. Am. 98, 1423-1445 (1995)]. To examine the influence of this notch, four Eptesicus were trained to discriminate between two sets of electronically generated artificial echoes. The negative (unrewarded) stimulus contained a test spectral notch at a specific frequency that varied from 30 to 50 kHz, while the positive (rewarded) stimulus contained no test notch. The vertical position of the loudspeakers delivering these simulated echoes was changed daily. When echoes were returned from an elevation at which the external ear introduced a spectral notch at the same frequency as the test notch, then the discrimination should have been difficult. The bats' performance conformed to this prediction: All bats discriminated the presence of a 35-kHz notch at all elevations except -10 degrees. As the frequency of the synthesized notch increased, the elevation at which bats could not perform the discrimination also increased. The movement of the bat's "blind spot" for the test notch of different frequencies followed the movement of the external ear notch at different elevations.

Representation of perceptual dimensions of insect prey during terminal pursuit by echolocating bats.

The echolocating big brown bat, Eptesicus fuscus, broadcasts brief frequency-modulated (FM) ultrasonic sounds and perceives objects from echoes of these sounds returning to its ears. Eptesicus is an insectivorous species that uses sonar to locate and track flying prey. Although the bat normally hunts in open areas, it nevertheless is capable of chasing insects into cluttered environments such as vegetation, where it completes interceptions in much the same manner as in the open except that it has to avoid the obstacles as well as catch the insect. During pursuit, the bat shortens its sonar signals and increases their rate of emission as it closes in to seize the target, and it keeps its head pointed at the insect throughout the maneuver. In the terminal stage of interception, the bat makes rapid adjustments in its flight-path and body posture to capture the insect, and these reactions occur whether the bat is pursuing its prey in the open or close to obstacles such as vegetation. Insects can be distinguished from other objects by the spectrum and phase of their echoes, and Eptesicus is very good at discriminating these acoustic features. To identify the insect in the open, but especially to distinguish which object is the insect in clutter, the bat must have some means for representing these features throughout the interception maneuver. Moreover, continuity for perception of these features is necessary to keep track of the prey in complex surroundings, so the nature of the auditory representations for the spectrum and phase of echoes has to be conserved across the approach, tracking, and terminal stages. The first problem is that representation of changes in the phase of echoes requires neural responses in the bat's auditory system to have temporal precision in the microsecond range, which seems implausible from conventional single-unit studies in the bat's inferior colliculus, where the temporal jitter of responses typically is hundreds of microseconds. Another problem is that echoes do not explicitly evoke neural responses in the inferior colliculus distinct from responses evoked by the broadcast during the terminal stage because the delay of echoes is too short for responsiveness to recover from the emissions. In contrast, each emission and each echo evokes its own responses during the approach and tracking stages of pursuit. How does the bat consistently represent the phase of echoes in spite of these evident limitations in neural responses? Local multiunit responses recorded from the inferior colliculus of Eptesicus reveal a novel format for encoding the phase of echoes at all stages of interception. Changes in echo phase (0 degree or 180 degrees) produce shifts in the latency of responses to the emission by hundreds of microseconds, an unexpected finding that demonstrates the existence of expanded time scales in neural responses representing the target at all stages of pursuit.