Activation in the auditory pathway of the gerbil studied with 18F-FDG PET: effects of anesthesia.

Here, we present results from an 18F-fluorodeoxyglucose (18F-FDG) positron emission tomography (PET) study in the Mongolian gerbil, a preferred animal model in auditory research. One major issue in preclinical nuclear imaging, as well as in most of the neurophysiological methods investigating auditory processing, is the need of anesthesia. We compared the usability of two types of anesthesia which are frequently employed in electrophysiology, ketamine/xylazine (KX), and fentanyl/midazolam/medetomidine (FMM), for valid measurements of auditory activation with 18F-FDG PET. Gerbils were placed in a sound-shielding box and injected with 18F-FDG. Two acoustic free-field conditions were used: (1) baseline (no stimulation, 25 dB background noise) and (2) 90 dB frequency-modulated tones (FM). After 40 min of 18F-FDG uptake, a 30 min acquisition was performed using a small animal PET/CT system. Blood glucose levels were measured after the uptake phase before scanning. Standardized uptake value ratios for relevant regions were determined after implementing image and volume of interest templates. Scans demonstrated a significantly higher uptake in the inferior colliculus with FM stimulation compared to baseline in awake subjects (+ 12%; p = 0.02) and with FMM anesthesia (+ 13%; p = 0.0012), but not with KX anesthesia. In non-auditory brain regions, no significant difference was detected. Blood glucose levels were significantly higher under KX compared to FMM anesthesia (17.29 ± 0.42 mmol/l vs. 14.30 ± 1.91 mmol/l; p = 0.024). These results suggest that valid 18F-FDG PET measurements of auditory activation comparable to electrophysiology can be obtained from gerbils during opioid-based anesthesia due to its limited effects on interfering blood glucose levels.

Analysis of spectral shape in the barn owl auditory system.

In a behavioral experiment, we investigated how efficiently barn owls (Tyto alba) could detect changes in the spectral profile of multi-component auditory signals with stochastic envelope patterns. Signals consisted of one or five bands of noise (bandwidth 4, 16, or 64 Hz each; center frequencies 1.02, 1.43, 2.0, 2.8, 3.92 kHz). We determined increment thresholds for the 2 kHz component for three conditions: single-band condition (only the 2 kHz component), all five noise bands with the envelope fluctuations of the bands being either correlated or uncorrelated. Noise bandwidth had no significant effect on increment detection. Increment thresholds for the different conditions, however, differed significantly. Thresholds in correlated conditions were generally the lowest of all conditions, whereas, thresholds in uncorrelated conditions mostly resulted in the highest thresholds. This can be interpreted as evidence for comodulation masking release in barn owls. If the increment in the 2 kHz component is balanced by decrementing the four flanking bands in amplitude, increment detection thresholds are not affected. The data suggest that the barn owls used information from simultaneous spectral comparison across different frequency channels to detect spectral changes in multi-component noise signals rather than sequential comparison of overall stimulus levels.

Release from masking in fluctuating background noise in a songbird's auditory forebrain.

Fluctuations in the ubiquitous masking background noise can be exploited by the vertebrate auditory system to considerably improve signal detection. Here we demonstrate neuronal masking release in amplitude-modulated background noise on the level of the European starling's auditory forebrain, an area that is the analogue of the mammalian primary auditory cortex. Tone-evoked responses in the presence of modulated and unmodulated maskers were recorded in unrestrained birds via radiotelemetry. Based on a rate code, the average amount of neuronal masking release was similar to that observed in a psychoacoustic study on the starling with stimuli confined to a single auditory filter. The results suggest that the neurons exploited predominantly temporal features of the acoustic background to improve signal detection.

Signal detection in amplitude-modulated maskers. II. Processing in the songbird's auditory forebrain.

In the natural environment, acoustic signals have to be detected in ubiquitous background noise. Temporal fluctuations of background noise can be exploited by the auditory system to enhance signal detection, especially if spectral masking components are coherently amplitude modulated across several auditory channels (a phenomenon called 'comodulation masking release'). In this study of neuronal mechanisms of masking release in the primary auditory forebrain (field L) of awake European starlings (Sturnus vulgaris), we determined and compared neural detection thresholds for 20-ms probe tones presented in a background of sinusoidally amplitude modulated (10-Hz) noise maskers. Responses of a total of 34 multiunit clusters were recorded via radiotelemetry with chronically implanted microelectrodes from unrestrained birds. For maskers consisting of a single noise band centred around the recording site's characteristic frequency, a substantial reduction in detection threshold (21 dB on average) was found when probe tones were presented during envelope dips rather than during envelope peaks. Such effects could also explain results obtained for masking protocols where the on-frequency noise band was presented together with excitatory or inhibitory flanking bands that were either coherently modulated (in-phase) or incoherently modulated (phase-shifted). Generally, masking release for probe tones in maskers with flanking bands extending beyond the frequency range of a cell cluster's excitatory tuning curve was not substantially improved. Only some of the neurophysiological results are in agreement with behavioural data from the same species if only the average population response is considered. A subsample of individual neurons, however, could account for behavioural thresholds.

Time course of simultaneous masking in the starling's auditory forebrain.

Simultaneous masking of pure tones was studied in the primary auditory forebrain of a songbird species, the European starling (Sturnus vulgaris). The responses of 32 multi-unit clusters in the input layer of the auditory neostriatum (field L2a) were recorded via radiotelemetry from freely moving birds. The probe was a 10-ms tone burst at the units' characteristic-frequency (CF) presented 20 dB above the threshold. The masker was an 80-ms tone burst presented either at the units' CF (excitatory masker) or at a frequency located in inhibitory side-bands (inhibitory masker) of the units' tuning curves. The probe was presented either 3 ms or 63 ms after masker onset. Probes presented at a 3-ms delay were influenced at significantly lower levels of an excitatory masker than probes presented at a 63-ms delay. The mean difference in masker level at the detection thresholds for both probe delays was 8 dB. No difference in masker level was observed for inhibitory-frequency maskers. The observed neural masking effects may be explained by at least four mechanisms: (1) swamping of the probe response by the response to the masker, (2) a reduction of the probe response during neural adaptation of the response to the masker, (3) a reduction of the probe response during side-band inhibition in the central nervous system, and (4) suppression originating in the cochlea.

Adjustable frequency selectivity of auditory forebrain neurons recorded in a freely moving songbird via radiotelemetry.

One of the hearing system's basic properties that determines the detection of signals is its frequency selectivity. In the natural environment, a songbird may achieve an improved detection ability if the neuronal filters of its auditory system could be sharpened to adapt to the spectrum of the background noise. To address this issue, we studied 35 multi-unit clusters in the input layer of the primary auditory forebrain of nine European starlings (Sturnus vulgaris). Microelectrodes were chronically implanted in this songbird's cortex analogue and the neuronal activity was transmitted from unrestrained birds via a miniature FM transmitter. Frequency tuning curves (FTCs) and inhibitory sidebands were determined by presenting a matrix of frequency-level combinations of pure tones. From each FTC, the characteristic frequency (CF) and several parameters describing the neurons' filter characteristics were derived and compared to the same recording site's filter function while simultaneously stimulating with a continuous CF tone 20 dB above the response threshold. Our results show a significant improvement of frequency selectivity during two-tone stimulation, indicating that spectral filtering in the starling's auditory forebrain depends on the acoustic background in which a signal is presented. Moreover, frequency selectivity was found to be a function of the time over which the stimulus persisted, since FTCs were much sharper and inhibitory sidebands were largely expanded several milliseconds after response onset. Neuronal filter bandwidths during two-tone stimulation in the auditory forebrain are in good agreement with psychoacoustically measured critical bandwidths in the same species. Radiotelemetry proved to be a powerful tool in studying neuronal activity in freely behaving birds.

Critical bands and critical-ratio bandwidth in the European starling.

Critical bands (CB) and critical-ratio (CR) bandwidth were determined in five European starlings (Sturnus vulgaris) using a GO/NOGO procedure and the method of constant stimuli. Test-tone frequencies were 1, 2, 4, and 6.3 kHz. Critical ratios were independent of the level of the white noise masker. The lowest CR of 21.8 dB was found at 1 kHz, and the CR monotonically increased on average by 2.3 dB per octave. CR-bandwidths at a masker spectrum level of 41 dB were 151, 191, 437, and 501 Hz at 1, 2, 4, and 6.3 kHz, respectively. With the exception of the test-tone frequency of 6.3 kHz, the size of the critical bands measured with a band-narrowing procedure was similar to that of the CR-bandwidth. CBs were 135, 233, 345, and 1156 Hz at 1, 2, 4, and 6.3 kHz, respectively. A repeat measurement at 6.3 kHz with another speaker position yielded a CB of 860 Hz. The results of this psychoacoustic study in the starling are discussed with respect to comparative data from other vertebrates and to neurophysiological bandwidth measurements of tuning curves of auditory-nerve fibres.

Peripheral basis for the auditory deficit in Belgian Waterslager canaries (Serinus canarius).

Recently, behavioural thresholds obtained in canaries of the Belgian Waterslager strain showed that these birds have an inherited auditory deficit. Canaries of this strain have absolute auditory thresholds at frequencies above 2.0 kHz that are as much as 40 dB above the threshold of canaries of other strains. We obtained audiograms from cochlear microphonics and from compound action potentials from the 8th nerve of Waterslager and non-Waterslager canaries and compare these results to previous behavioural data on hearing in this species. We also examined the growth of evoked potential amplitude-intensity functions in Waterslager and non-Waterslager canaries. Together with reflectance measurements of middle-ear function from both Waterslager and non-Waterslager canaries, we conclude that the origin of auditory deficit in Waterslager canaries lies in the cochlea.

Temporal modulation transfer functions in the European Starling (Sturnus vulgaris): II. Responses of auditory-nerve fibres.

The temporal resolution of cochlear-nerve fibres in the European starling was determined with sinusoidally amplitude-modulated noise stimuli similar to those previously used in a psychoacoustic study in this species (Klump and Okanoya, 1991). Temporal modulation transfer curves (TMTFs) were constructed for cochlear afferents allowing a direct comparison with the starling's behavioural performance. On average, the neuron's detection of modulation was less sensitive than that obtained in the behavioural experiments, although the most sensitive cells approached the values determined psychophysically. The shapes of the neural TMTFs generally resembled low-pass or band-pass filter functions, and the shapes of the averaged neural functions were very similar to those obtained in the behavioural study for two different types of stimuli (gated and continuous carrier). Minimum integration times calculated from the upper cut-off frequency of the neural TMTFs had a median of 0.97 ms with a range of 0.25 to 15.9 ms. The relations between the minimum integration times and the tuning characteristics of the cells (tuning curve bandwidth, Q10 dB-value, high- and low-frequency slopes of the tuning curves) are discussed. Finally, we compare the TMTF data recorded in the starling auditory nerve with data from neurophysiological and behavioural observations on temporal resolution using other experimental paradigms in this and other vertebrate species.

Temporal modulation transfer functions in the European starling (Sturnus vulgaris): I. Psychophysical modulation detection thresholds.

Temporal modulation transfer functions (TMTF) were obtained from four European starlings (Sturnus vulgaris) using a psychophysical Go/NoGo procedure combined with the method of constant stimuli. The TMTF for a continuous, broad-band noise of 55 dB SPL had a low-pass characteristic with a cut-off frequency of 123 Hz. For an 800 ms gated stimulus of the same sound-pressure level, the TMTF had the shape of a band-pass filter with the most sensitive modulation frequency at around 20 Hz. At 75 dB the band-pass shape of the TMTF was preserved, whereas at 35 dB SPL the TMTF had a low-pass characteristic. The cut-off frequency of the TMTF for continuous noise depends on which part of the spectrum carries the information on the envelope fluctuations. If only sound energy below 1 or 1.5 kHz is modulated, then the cut-off frequencies are 40 and 38 Hz, respectively. If only sound above 3 kHz carries the information on the modulation, then the cut-off frequency is 125 Hz and the shape of the TMTF is similar to that found for broadband noise. The results are discussed with respect to the coding of sinusoidal amplitude modulations by the auditory system and to different measures of time, frequency and intensity resolution in the starling.