Long-range cortical synchronization without concomitant oscillations in the somatosensory system of anesthetized cats.

To determine whether neuronal oscillations are essential for long-range cortical synchronization in the somatosensory system, we characterized the incidence and response properties of gamma range oscillations (20-80 Hz) among pairs of synchronized neurons in primary (SI) and secondary (SII) somatosensory cortex. Synchronized SI and SII discharges, which occurred within a 3 msec period, were detected in 13% (80 of 621) of single-unit pairs and 25% (29 of 118) of multiunit pairs. Power spectra derived from the auto-correlation histograms (ACGs) revealed that approximately 15% of the neurons forming synchronized pairs were characterized by oscillations. Although 24% of the synchronized neuron pairs (19/80) were characterized by oscillations in one or both neurons, only 1% (1/80) of these pairs displayed oscillations at the same frequency in both neurons. Similar results were observed among pairs of multiunit responses. When single-trial responses were analyzed, the vast majority of responses still did not exhibit oscillations in the gamma frequency range. These results suggest that separate populations of cortical neurons can be bound together without being constrained by the phase relationships defined by specific oscillatory frequencies.

Synchronized cortical potentials and wavelet packets: a potential mechanism for perceptual binding and conveying information.

Temporal synchronization in neuronal assemblies has been linked to the functional roles of perceptual binding, sensory-motor integration, attention, and information coding. We report new evidence for a common underlying mechanism that uses specific temporal patterns of synchronized neuronal activity as a basis for conveying information. The temporal patterns of stimulus-related synchronized neuronal discharges are structured to closely resemble specific members of the Symlet wavelet packet family employed in a computational framework. Together, these results suggest that temporal patterns of synchronized activity may act as a parallel, distributed code for information through a mechanism computationally equivalent to wavelet packet analysis.

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.

Delay-tuned neurons in the midbrain of the big brown bat.

1. The auditory midbrain in Eptesicus contains delay-tuned neurons that encode target range. Most delay-tuned neurons respond poorly to tones or individual frequency-modulated (FM) sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned. The index of facilitation (IF), a coefficient measuring combination sensitivity for individual delay-tuned neurons, ranged from 0.14 to 1.0, with an average of 0.64 +/- 0.24 (mean +/- SD). Of the 33 facilitated responses from 29 neurons, 23 (70%) exhibited IFs > 0.5, which corresponds to a facilitated response 3 times greater than the sum of the responses to individual pulse and echoes. Thus the responses of midbrain delay-tuned neurons are highly combination sensitive. 2. The response of midbrain delay-tuned neurons is phasic, with an average of 0.7 +/- 0.4 action potentials elicited per optimal pulse-echo pair. Thus midbrain delay-tuned neurons in Eptesicus act as probability encoders. 3. The distribution of best echo delays (BDs) of midbrain delay-tuned neurons ranged from 8 to 30 ms. As an ensemble, midbrain delay-tuned neurons encode target ranges of 138-516 cm. There is a basic correspondence between the physiologically determined span of midbrain BDs between 8 and 30 ms and the behaviorally determined borders of the approach (8- to 17-ms echo delay) and search stages (17- to 30-ms echo delay) of the insect pursuit sequence. Midbrain delay-tuned neurons can be separated into two subpopulations on the basis of the difference in distributions of the echo best amplitude (EBA) tuning at BD. The BDs of one subpopulation correspond to the span of search stage echo delays, and the BDs of the other subpopulation correspond to the span of approach stage echo delays. 4. EBAs of neurons in each subpopulation are tailored to the specific perceptual requirements of the corresponding behavioral stage. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 12) correspond to the search stage and are suited to the requirements of target detection. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 21) correspond to the approach stage and are suited to the requirements of target size discrimination. 5. The best FM sweeps for the pulse (PFM) and echo (EFM) were determined for each midbrain neuron. PFMs appear to cluster at frequencies corresponding to the three harmonic peaks in the emitted pulse power spectra.(ABSTRACT TRUNCATED AT 400 WORDS)

A computational model of echo processing and acoustic imaging in frequency-modulated echolocating bats: the spectrogram correlation and transformation receiver.

The spectrogram correlation and transformation (SCAT) model of the sonar receiver in the big brown bat (Eptesicus fuscus) consists of a cochlear component for encoding the bat's frequency modulated (FM) sonar transmissions and multiple FM echoes in a spectrogram format, followed by two parallel pathways for processing temporal and spectral information in sonar echoes to reconstruct the absolute range and fine range structure of multiple targets from echo spectrograms. The outputs of computations taking place along these parallel pathways converge to be displayed along a computed image dimension of echo delay or target range. The resulting image depicts the location of various reflecting sources in different targets along the range axis. This series of transforms is equivalent to simultaneous, parallel forward and inverse transforms on sonar echoes, yielding the impulse responses of targets by deconvolution of the spectrograms. The performance of the model accurately reproduces the images perceived by Eptesicus in a variety of behavioral experiments on two-glint resolution in range, echo phase sensitivity, amplitude-latency trading of range estimates, dissociation of time- and frequency-domain image components, and ranging accuracy in noise.

Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus.

1. In Eptesicus the auditory cortex, as defined by electrical activity recorded from microelectrodes in response to tone bursts, FM sweeps, and combinations of FM sweeps, encompasses an average cortical surface area of 5.7 mm2. This area is large with respect to the total cortical surface area and reflects the importance of auditory processing to this species of bat. 2. The predominant pattern of organization in response to tone bursts observed in each cortex is tonotopic, with three discernible divisions revealed by our data. However, although cortical best-frequency (BF) maps from most of the individual bats are similar, no two maps are identical. The largest division contains an average of 84% of the auditory cortical surface area, with BF tonotopically mapped from high to low along the anteroposterior axis and is part of the primary auditory cortex. The medium division encompasses an average of 13% of the auditory cortical surface area, with highly variable BF organization across bats. The third region is the smallest, with an average of only 3% of auditory cortical surface area and is located at the anterolateral edge of the cortex. This region is marked by a reversal of the tonotopic axis and a restriction in the range of BFs as compared with the larger, tonotopically organized division. 3. A population of cortical neurons was found (n = 39) in which each neuron exhibited two BF threshold minima (BF1 and BF2) in response to tone bursts. These neurons thus have multipeaked frequency threshold tuning curves. In Eptesicus the majority of multipeaked frequency-tuned neurons (n = 27) have threshold minima at frequencies that correspond to a harmonic ratio of three-to-one. In contrast, the majority of multipeaked neurons in cats have threshold minima at frequencies in a ratio of three-to-two. A three-to-one harmonic ratio corresponds to the "spectral notches" produced by interference between overlapping echoes from multiple reflective surfaces in complex sonar targets. Behavioral experiments have demonstrated the ability of Eptesicus to use spectral interference notches for perceiving target shape, and this subpopulation of multipeaked frequency-tuned neurons may be involved in coding of spectral notches. 4. The auditory cortex contains delay-tuned neurons that encode target range (n = 99). Most delay-tuned neurons respond poorly to tones or individual FM sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned.(ABSTRACT TRUNCATED AT 400 WORDS)

A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat.

Behavioural studies and field observations demonstrate that echolocating bats simultaneously perceive range, direction and shape of multiple objects in the environment as acoustic images derived from echoes. Cortical echo delay-tuned neurons contribute to the perception of object range, because focal inactivation of these neurons disrupts behavioural discrimination of range. We report here that response properties of delay-tuned neurons in the cortical tonotopic area of the bat, Eptesicus, transform the sequential arrival times of echoes with different delays into a concurrent, accumulating neural representation of multiple objects at different ranges. The sharpness of delay tuning systematically increases at each best delay in a subpopulation of these neurons while responses to echoes at different delays are accumulated. The resulting concurrent, multiresolution representation of echo delay corresponds to neural implementation of a common representation of images used in computational vision and may provide the basis for representing acoustic images of multiple objects as acoustic 'scenes'.

Middle ear structure in the chinchilla: a quantitative study.

The anatomic features of the chinchilla middle ear were identified and various aspects of the conductive apparatus were measured in a number of specimens by different methods. These aspects included area measures of the tympanic membrane, stapes footplate, oval window, and round window; middle-ear volume; dimensions of the ossicles, the length of their rotational axes as well as the malleus to incus lever ratio. We also weighed the ossicles. The findings are discussed with reference to their possible significance for auditory signal processing in the chinchilla.

The anatomical consequences of acoustic injury: A review and tutorial.

The anatomic consequences of acoustic overstimulation are explored in this presentation, and attention is directed toward issues where improvements in technology and empirical observation are needed before further advances in our understanding can be achieved. Gains have been made in the last decade in appreciating sound-induced cochlear injury, but there is now a need to evaluate not only cochlear pathology but also the functional state of the surviving structures. There is a wealth of information about the susceptibility of inner or outer hair cells to acoustic injury; however, the etiology of this injury is not yet fully understood. In addition, current ideas concerning the effects of noise on hair-cell stereocilia, hair-cell synapses, the cochlear vascular supply, and the central auditory pathways are in a state of flux and are either undergoing revision or emerging. Other issues, such as the basis of temporary or permanent threshold shift at the cellular level, and the individual differences in susceptibility to injury are in need of a fresh approach. It would seem that the time is now ripe to review our knowledge, recognize its gaps, and develop testable hypotheses concerning the mechanisms of acoustic injury to the ear.

The structure and function of actin in hair cells.

Within the last 7 years, the protein actin has been identified in the stereocilia and cuticular plate region of the hair cell. An intensive effort has been mounted to describe the structural organization of this protein, to identify actin-associated proteins in these regions, and to identify the functional role of these proteins. The paracrystalline array of actin and its cross bridges imparts rigidity and stiffness to the stereocilia, which are important in determining their response properties. It also appears that these properties can be changed if the paracrystalline array is damaged by noise exposure. The functional implications of stereocilia rigidity and stiffness, as well as potential contractile mechanisms in the hair cell, are discussed. Finally, it is suggested that changes in the cross-sectional shape of the stereocilia caused by shearing of actin filaments during stereocilia deflections can be related to the mechano-electrical events in the plasma membrane of the cell. This may be the link between the transmission of vibrational energy through the sensory accessory structures of the peripheral ear, and the initiation of electrochemical events associated with transduction.