Coding of Small Sinusoidal Frequency and Amplitude Modulations in the Inferior Colliculus of 'CF-FM' Bat, Rhinolophus Ferrumequinum

Single neurons in the inferior colliculus of the Greater Horseshoe bat, Rhinolophus ferrumequinum, showed two broad categories of response patterns to sinusoidally frequency (SFM) or amplitude (SAM) modulated stimuli. Tonic responding cells (best excitatory frequency (BEF) between 10 and 90 kHz) showed a rough sinusoidal modulation of the discharge pattern to SFM. Transient responding neurons, generally showing on- or off-responses to pure tones, (BEF between 65 and 88 kHz), displayed highly synchronized discharge patterns to SFM-cycles (Fig. 1). Modulation rates between 20 and 100 Hz were most effective and some neurons encoded modulation rates up to 350 Hz (Figs. 2 and 3). The SFM responses were best synchronized to the modulation envelope for center frequencies in the upper portion of the tuning curve (Figs. 4 and 5). Sharply tuned neurons with BEF around 80 kHz had the lowest threshold for modulation depth (± 10 Hz or 0.025%) (Fig. 6). In general, SAMs evoked the same type of response patterns and were encoded down to modulation index of 3% (Fig. 7). The fine frequency and amplitude discriminations for periodical modulations by collicular neurons is discussed as related to the detection and discrimination performance of bats, when preying on flying insects in clustered surroundings

Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus f errumequinum

1. Acoustic reflections from a wing beating moth to an 80 kHz ultrasonic signal were recorded from six different incident angles and analyzed in spectral and time domains. The recorded echoes as well as independent components of amplitude and frequency modulations of the echoes were employed as acoustic stimuli during single unit studies. 2. The responses of single inferior colliculus neurons to these stimuli were recorded from four horseshoe bats,Rhinolophus ferrumequinum, a species which uses a long constant frequency (CF) sound with a final frequency modulated (FM) sweep during echolocation. All neurons responding to wing beat echoes reliably encoded the fundamental wing beat frequency as well as the more refined frequency and amplitude modulations. 3. These neurons may provide the bat a neural mechanism to detect periodically moving targets against a cluttered background and also to discriminate various insect species on the basis of their wing beat patterns

Encoding of Temporal Sound Features in the Rodent Superior Paraolivary Nucleus

The superior paraolivary nucleus (SPON) is a prominent cell group in the mammalian brainstem. SPON neurons are part of a monaural circuit that encodes temporal sound features in the ascending auditory pathway. Such attributes of acoustic signals are critical for speech perception in humans and likely equally as important in animal communication. While basic properties of SPON neurons have been characterized in some detail, a comprehensive examination of mechanisms that underlie their ability to precisely represent temporal information is lacking. Furthermore, little is known of how the SPON impacts its primary target, the inferior colliculus. Combinations of electrophysiological, pharmacological and histological techniques were used to investigate SPON neuronal responses to stimuli whose temporal parameters were systematically varied. In addition, properties of neurons in the inferior colliculus were examined before and after reversible inactivation of the SPON in order to explore its functional role in hearing. An after-hyperpolarization rebound mechanism was shown to generate the hallmark offset response of SPON neurons in vitro. Single-cell labeling techniques provided a detailed morphological description of cell bodies and dendrites and revealed a homogeneous population of neurons. Moreover, subthreshold ionic currents and synaptic neurotransmitter receptor systems were shown to mediate the precision of responses to temporal features of sound in vivo. It was also demonstrated that input from the SPON shapes response properties of inferior colliculus neurons to both periodic and singular temporal stimulus features. Taken together, these results suggest the SPON likely has a substantial role in temporal processing that has not been taken into account in the current understanding of the central auditory system. Demonstrating a functional role for the SPON in hearing will expand our knowledge of neuronal circuits responsible for representing biologically important sounds in both normal hearing and hearing impaired states

Neuronal Sensitivity to Microsecond Time Disparities in the Electrosensory System of Gymnarchus niloticus

To perform the jamming avoidance response (JAR), the weakly electric fish Gymnarchus detects time disparities on the order of microseconds between electrosensory signals received by electroreceptors in different parts of the body surface. This paper describes time-disparity thresholds of output neurons of the electrosensory lateral line lobe (ELL), where the representation of timing information is converted from a time code to a firing-rate code. We recorded extracellular single-unit responses from pyramidal cells in the ELL to sinusoidally modulated time disparity with various depths (0-200 μs). Threshold sensitivity to time disparities measured in 123 units ranged from 0.5 to 100 μs and was ≤5 μs in 60% of the units. The units from pyramidal cells in the inner and outer cell layers of the ELL responded equally well to small time disparities. The neuronal thresholds to time disparities found in the ELL are comparable with those demonstrated in behavioral performance of the JAR. The sensitivity of ELL units to small time disparities was unaffected when the center of the cyclic time-disparity modulation was shifted over a wide range (up to 250 μs), indicating an adaptation mechanism for steady-state time disparities that preserves the sensitivity to small dynamic changes in time disparities. Phase-locked input neurons, which provide time information to the ELL by phase-locked firing of action potentials, did not adapt to steady-state time shifts of sensory signals. This suggests that the adaptation emerges within the ELL

Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus f errumequinum

1. Acoustic reflections from a wing beating moth to an 80 kHz ultrasonic signal were recorded from six different incident angles and analyzed in spectral and time domains. The recorded echoes as well as independent components of amplitude and frequency modulations of the echoes were employed as acoustic stimuli during single unit studies. 2. The responses of single inferior colliculus neurons to these stimuli were recorded from four horseshoe bats,Rhinolophus ferrumequinum, a species which uses a long constant frequency (CF) sound with a final frequency modulated (FM) sweep during echolocation. All neurons responding to wing beat echoes reliably encoded the fundamental wing beat frequency as well as the more refined frequency and amplitude modulations. 3. These neurons may provide the bat a neural mechanism to detect periodically moving targets against a cluttered background and also to discriminate various insect species on the basis of their wing beat patterns

Neural coding of pitch cues in the auditory midbrain of unanesthetized rabbits

Pitch is an important attribute of auditory perception that conveys key features in music, speech, and helps listeners extract useful information from complex auditory environments. Although the psychophysics of pitch perception has been extensively studied for over a century, the underlying neural mechanisms are still poorly understood. This thesis examines pitch cues in the inferior colliculus (IC), which is the core processing center in the mammalian auditory midbrain that relays and transforms convergent inputs from peripheral brainstem nuclei to the auditory cortex. Previous studies have shown that IC can encode low-frequency fluctuations in stimulus envelope that are related to pitch, but most experiments were conducted in anesthetized animals using stimuli that only evoked weak pitch sensations and only investigated a limited frequency range. Here, we used single-neuron recordings from the IC in normal hearing, unanesthetized rabbits in response to a comprehensive set of complex auditory stimuli to explore the role of IC in the neural processing of pitch. We characterized three neural codes for pitch cues: a temporal code for the stimulus envelope repetition rate (ERR) below 900 Hz, a rate code for ERR between 60 and 1600 Hz, and a rate-place code for frequency components individually resolved by the cochlea that is mainly available above 800 Hz. While the temporal code and the rate-place code are inherited from the auditory periphery, the rate code for ERR has not been currently characterized in processing stages prior to the IC. To help interpret our experimental findings, we used computational models to show that the IC rate code for ERR likely arises via temporal interaction of multiple synaptic inputs, and thus the IC performs a temporal-to-rate code transformation from peripheral to cortical representations of pitch cues. We also show that the IC rate-place code is robust across a 40 dB range of sound levels, and is likely strengthened by inhibitory synaptic inputs. Together, these three codes could provide neural substrates for pitch of stimuli with various temporal and spectral compositions over the entire frequency range

Sensitivity to interaural time differences in the medial superior olive of a small mammal, the Mexican free-tailed bat

Neurons in the medial superior olive (MSO) are thought to encode interaural time differences (ITDs), the main binaural cues used for localizing low-frequency sounds in the horizontal plane. The underlying mechanism is supposed to rely on a coincidence of excitatory inputs from the two ears that are phase-locked to either the stimulus frequency or the stimulus envelope. Extracellular recordings from MSO neurons in several mammals conform with this theory. However, there are two aspects that remain puzzling. The first concerns the role of the MSO in small mammals that have relatively poor low-frequency hearing and whose heads generate only very small ITDs. The second puzzling aspect of the scenario concerns the role of the prominent binaural inhibitory inputs to MSO neurons. We examined these two unresolved issues by recording from MSO cells in the Mexican free-tailed bat. Using sinusoidally amplitude-modulated tones, we found that the ITD sensitivities of many MSO cells in the bat were remarkably similar to those reported for larger mammals. Our data also indicate an important role for inhibition in sharpening ITD sensitivity and increasing the dynamic range of ITD functions. A simple model of ITD coding based on the timing of multiple inputs is proposed. Additionally, our data suggest that ITD coding is a by-product of a neuronal circuit that processes the temporal structure of sounds. Because of the free-tailed bat's small head size, ITD coding is most likely not the major function of the MSO in this small mammal and probably other small mammals

Responses to Diotic, Dichotic, and Alternating Phase Harmonic Stimuli in the Inferior Colliculus of Guinea Pigs

Humans perceive a harmonic series as a single auditory object with a pitch equivalent to the fundamental frequency (F0) of the series. When harmonics are presented to alternate ears, the repetition rate of the waveform at each ear doubles. If the harmonics are resolved, then the pitch perceived is still equivalent to F0, suggesting the stimulus is binaurally integrated before pitch is processed. However, unresolved harmonics give rise to the doubling of pitch which would be expected from monaural processing (Bernstein and Oxenham, J. Acoust. Soc. Am., 113:3323–3334, 2003). We used similar stimuli to record responses of multi-unit clusters in the central nucleus of the inferior colliculus (IC) of anesthetized guinea pigs (urethane supplemented by fentanyl/fluanisone) to determine the nature of the representation of harmonic stimuli and to what extent there was binaural integration. We examined both the temporal and rate-tuning of IC clusters and found no evidence for binaural integration. Stimuli comprised all harmonics below 10 kHz with fundamental frequencies (F0) from 50 to 400 Hz in half-octave steps. In diotic conditions, all the harmonics were presented to both ears. In dichotic conditions, odd harmonics were presented to one ear and even harmonics to the other. Neural characteristic frequencies (CF, n = 85) were from 0.2 to 14.7 kHz; 29 had CFs below 1 kHz. The majority of clusters responded predominantly to the contralateral ear, with the dominance of the contralateral ear increasing with CF. With diotic stimuli, over half of the clusters (58%) had peaked firing rate vs. F0 functions. The most common peak F0 was 141 Hz. Almost all (98%) clusters phase locked diotically to an F0 of 50 Hz, and approximately 40% of clusters still phase locked significantly (Rayleigh coefficient >13.8) at the highest F0 tested (400 Hz). These results are consistent with the previous reports of responses to amplitude-modulated stimuli. Clusters phase locked significantly at a frequency equal to F0 for contralateral and diotic stimuli but at 2F0 for dichotic stimuli. We interpret these data as responses following the envelope periodicity in monaural channels rather than as a binaurally integrated representation