Neural responses in the inferior colliculus of echolocating bats to artificial orientation sounds and echoes

The responses of single units and evoked potentials to a pair of artificial sounds, mimicking theorientation sound and echo, and to tape recorded actual orientation sounds were studied in terms of recovery cycle. the recovery cycle of single units could be classified into four groups: (1) short suppression (4%), (2) delayed inhibition (11%), (3) temporal recovery with or without a supernormal phase (7%), and (4) undelayed inhibition (78%) lasting 4 to 26 msec. therefore the majority of neurons were not excited by the second sound (echo) of a pair when it was delivered within several milliseconds after the first (out-going orientation sound). the duration of the recovery cycle was a function of the intensity of a pair of sounds. the weaker the first tone pulse relative to the second, the more rapid the recovery to the second. therefore, the reception of echoes is probably improved by contraction of middle ear muscles resulting in attenuation of self-stimulation by the out-going pulse. The collicular evoked potential consisted of two components, a fast one mainly due to the incoming fibers from lower levels and a slow one due to the main body of the inferior colliculus. The slow component showed slow recovery cycles as did the majority of single units while the fast one recovered very quickly. No noticeable difference in recovery cycles was found between awake and anesthetized animals. The functional meaning of inhibitory periods in the recovery cycle and role of the inferior colliculus in echo-location are discussed.     

Effects of sound direction on the processing of amplitude-modulated signals in the frog inferior colliculus

Single-unit recordings were made from 143 neurons in the frog (Rana p. pipiens) inferior colliculus (IC) to investigate how free-field sound direction influenced neural responses to sinusoidal-amplitude-modulated (SAM) tone and/or noise. Modulation transfer functions (MTFs) were derived from 3 to 5 sound directions within 180° of frontal field. Five classes of MTF were observed: low-pass, high-pass, band-pass, multi-pass, and all-pass. For 64% of IC neurons, the MTF class remained unchanged when sound direction was shifted from contralateral 90° to ipsilateral 90°. However, the MTFs of more than half of these neurons exhibited narrower bandwidths when the loudspeaker was shifted to ipsilateral azimuths. There was a decrease in the cut-off frequency for neurons possessing low-pass MTFs, an increase in cut-off frequency for neurons showing high-pass MTFs, or a reduction in the pass-band for neurons displaying bandpass MTFs. These results suggest that sound direction can influence amplitude modulation (AM) frequency tuning of single IC neurons.Since changes in periodicity of SAM tones alter both the temporal parameters of sounds as well as the sound spectrum, we examined whether directional effects on spectral selectivity play a role in shaping the observed direction-dependent AM selectivity. The directional influence on AM selectivity to both SAM tone and SAM noise was measured in 62 neurons in an attempt to gain some insight into the mechanisms that underlie directionally-induced changes in AM selectivity. Direction-dependent changes in the shapes of the tone and noise derived MTFs were different for the majority of IC neurons (55/62) tested. These data indicate that a spectrally-based and a temporally-based mechanism may be responsible for the observed results.Abbreviations AM amplitude modulation - CF characteristic frequency - DI direction index - FR isointensity frequency response - GABA gamma-aminobutyric acid - IC inferior colliculus - ICc central nucleus of the inferior colliculus - ITD interaural time difference - MTF modulation transfer function - PSTH peri-stimulus time histogram - SAM sinusoidal-amplitude-modulated - SC synchronization coefficient - CN cochlear nucleus     

Effects of GABA-mediated inhibition on direction-dependent frequency tuning in the frog inferior colliculus

Earlier studies from our laboratory have shown that the frequency selectivity of neurons in the frog inferior colliculus is direction dependent. The goal of this study was to test the hypotheses that gamma-aminobutyric acid or GABA (but not glycine)-mediated synaptic inhibition was responsible for the direction-dependence in frequency tuning, and that GABA acted through creation of binaural inhibition. We performed single unit recordings and investigated the unit's free-field frequency tuning, and/or the unit's response to the interaural level differences (under dichotic stimulation), before and during local applications of antagonists specific to gamma-aminobutyric acid a and glycine receptors. Our results showed that application of bicuculline produced a broadening of free-field frequency tuning, and differential changes in free-field frequency tuning depending on sound direction, i.e., more pronounced at azimuths at which the unit exhibited narrower frequency tuning under the pre-drug condition, thereby typically abolishing direction dependence in tuning. Application of strychnine produced no change in frequency tuning. The results from dichotic stimulation further revealed that bicuculline typically elevated and/or flattened the unit's interaural-level-difference response function, indicating a reduction in the strength of binaural inhibition. Our study provides evidence that gamma-aminobutyric acid-mediated binaural inhibition is important for direction dependence in frequency tuning. Accepted: 24 July 1998     

Characteristics of borderline modulation frequencies in the differentiation of tonal and amplitude-modulated stimuli following the removal of the inferior colliculus in rats

Elaboration of differentiation between sound stimuli was carried out in 15 laboratory rats. After bilateral ablations of auditory inferior colliculi the border frequency of stimulus amplitude modulation was determined for all rats when they still could differentiate between tonal and amplitude-modulated stimuli. Decrease in frequency of modulation by 2 Hz and more from the border frequency caused a complete loss of ability to differentiate. In all rats bilateral inferior colliculi ablations completely disturbed differentiation between tonal and amplitude-modulated signals with modulation frequency below 183-191 Hz (the range of border frequencies). The surgery however did not affect differentiation between tonal and amplitude-modulated signals with the modulation frequencies above 183-191 Hz. The data suggest that the functions of completion of coding of amplitude-modulated stimuli in the auditory system is strictly linked with definite structures.     

Serotonin modulates responses to species-specific vocalizations in the inferior colliculus

Neuromodulators such as serotonin are capable of altering the neural processing of stimuli across many sensory modalities. In the inferior colliculus, a major midbrain auditory gateway, serotonin alters the way that individual neurons respond to simple tone bursts and linear frequency modulated sweeps. The effects of serotonin are complex, and vary among neurons. How serotonin transforms the responses to spectrotemporally complex sounds of the type normally heard in natural settings has been poorly examined. To explore this issue further, the effects of iontophoretically applied serotonin on the responses of individual inferior colliculus neurons to a variety of recorded species-specific vocalizations were examined. These experiments were performed in the Mexican free-tailed bat, a species that uses a rich repertoire of vocalizations for the purposes of communication as well as echolocation. Serotonin frequently changed the number of recorded calls that were capable of evoking a response from individual neurons, sometimes increasing (15% of serotonin-responsive neurons), but usually decreasing (62% of serotonin-responsive neurons), this number. A functional consequence of these serotonin-evoked changes would be to change the population response to species-specific vocalizations.     

Neural modulation in inferior colliculus and central auditory plasticity

The neural modulation in central auditory system plays an important role in perception and processing of sound signal and auditory cognition. The inferior colliculus (IC) is both a relay station in central auditory pathway and a sub-cortical auditory center doing the sound signal processing. IC is also modulated by the descending projections from the cortex and auditory thalamus, medial geniculate body, and these neural modulations not only can affect ongoing sound signal processing but can also induce plastic changes in IC.     

Single unit responses in the auditory center of the frog mesencephalon to amplitude-modulated tones

Responses of most single neurons of the torus semicircularis ofRana ridibunda to stimuli of characteristic frequency and with low (10–30%) sinusoidal amplitude modulation were considerably stronger than those of the same neurons to pure tones. Analysis of phase histograms synchronized with the period of modulation was used to study dependence of the response on the frequency of modulation. In some cells the degree of modulation of the phase histogram fell steadily with an increase in modulation frequency, but in others a maximum was found in the 10–20 Hz region. Usually modulations of the phase histogram were significantly greater than stimulus modulation. The phase angle between the maximum of stimulus amplitude and the maximum of the unit response increased as an approximately linear function of the increase in modulation frequency.N. N. Andreev Acoustic Institute, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 12, No. 3, pp. 264–271, May–June, 1980.     

Dependence of responses of central auditory neurons on the depth and rate of frequency modulation

Unit responses of the inferior colliculi of anesthetized albino rats to frequency-modulated stimuli were studied. The number of spikes and the pattern and duration of the unit discharges in response to frequency modulation in different directions were shown to depend on the depth and rate of modulation. With a change in the rate of frequency modulation the number of spikes in the discharge of individual neurons could increase, decrease, or remain constant. Neurons of the inferior colliculi give their material discharge at different rates of frequency modulation. A change in the depth and rate of modulation did not change the sensitivity of most neurons to the direction of the frequency change in the stimulus within the frequency range corresponding to the center of the excitatory zone of the unit response.     

Reflection of the release from masking effect in unit activity of the cat inferior colliculus

The effect of release from masking in unit activity of the inferior colliculus was studied in anesthetized cats. When series of cophasic and antiphasic clicks with varied interaural delay were used as stimuli, sensitivity to changes in the interaural phase shift within a narrow band of the spectrum of the signal close to the characteristic frequency was discovered in neurons with low characteristic frequencies (up to 2.6 kHz). The masking effect with cophasic and antiphasic noise was found to depend on the phase sensitivity of the neurons. The neurophysiological mechanisms of the release from masking effect are discussed.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 17, No. 4, pp. 463–468, July–August, 1985.     

Ascending and descending projections to the inferior colliculus in the rat

The ascending and descending projections to the central nucleus of the inferior colliculus (IC) were studied with the aid of retrograde transport of horseradish peroxidase (HRP). HRP-labelled cells were found in contralateral cochlear nuclei, where the majority of different cell types was stained. Few labelled cells were observed in the ipsilateral cochlear nuclei. HRP-positive neurones were found in all nuclei of the superior olivary complex on the ipsilateral side with the exception of the medial nucleus of the trapezoid body, which was never labelled either ipsilaterally or contralaterally. The largest concentration of HRP-labelled cells was usually observed in the ipsilateral superior olivary nucleus. Smaller numbers of labelled cells were present in contralateral nuclei of the superior olivary complex. Massive projections to the inferior colliculus were found from the contralateral and ipsilateral dorsal nucleus of the lateral lemniscus and ipsilateral ventral nucleus of the lateral lemniscus. Many neurones of the central and external nuclei of the contralateral inferior colliculus were labelled with HRP. Topographic organisation of the pathways ascending to the colliculus was expressed in the cochlear nuclei, lateral superior olivary nucleus and in the dorsal nucleus of the lateral lemniscus. HRP--positive cells were found in layer V of the ipsilateral auditory cortex, however, the evidence for topographic organisation was lacking.     

Collicular responses to the frequency modulated final part of echolocation sounds in Rhinolophus ferrum equinum

Summary Collicular evoked potentials in Rhinolophus ferrum equinum show very prominent responses to the final frequency modulated part of a acoustic stimulus, simulating the natural echolocation sound.     

Anatomical changes of the GABAergic system in the inferior colliculus of the genetically epilepsy-prone rat

The number of GABAergic neurons as determined by GAD immunocytochemistry and total neurons as determined from Nissl preparations were counted and classified at the light microscopic level in the inferior colliculus (IC) of the genetically epilepsy prone rat (GEPR) and the non-epileptic Sprague-Dawley (SD) strain of rat. GAD-positive neurons are abundant in the IC and a significant increase in the number of GAD-positive neurons occurs in the GEPR as compared to the SD in all three subdivisions. However, the most pronounced difference occurs in the ventral lateral portion of the central nucleus, where there is a selective increase in the small (200%) and medium-sized (90%) GABAergic somata (10-15 microns in diameter and 15-25 microns in diameter, respectively). As determined from Nissl preparations an increase in total numbers of neurons also occurs. Thus, a 100% increase in the number of small neurons and a 30% increase in the number of medium-sized neurons occur in the adult GEPR as compared to the SD rat. A statistically significant increase in the numbers of small neurons also occurred in the IC of the young GEPR. At 4 days of age, a 55% increase in the number of small neurons was found, and at 10 days of age this increase was 105%. The numbers of the medium and large neurons were similar in the older group of rats. These data suggest that the increase in cell number observed in the adult GEPR is not compensatory to the seizure activity, but may either be genetically programmed or be a failure of cell death. Based on other studies of genetic models of epilepsy, we propose that the additional GABAergic neurons may disinhibit excitatory projection neurons in the IC.     

Encoding repetition rate and duration in the inferior colliculus of the big brown bat,Eptesicus fuscus

1. Encoding of temporal stimulus parameters by inferior collicular (IC) neurons of Eptesicus fuscus was studied by recording their responses to a wide range of repetition rates (RRs) and durations at several stimulus intensities under free field stimulus conditions. 2. The response properties of 424 IC neurons recorded were similar to those reported in previous studies of this species. 3. IC neurons were classified as low-pass, band-pass, and high-pass according to their preference for RRs and/or durations characteristic of, respectively, search, approach, or terminal phases of echolocation. These neurons selectively process stimuli characteristic of the various phases of hunting. 4. Best RRs and best durations were not correlated with either the BFs or recording depths This suggests that each isofrequency lamina is capable of processing RRs and durations of all hunting phases. 5. Responses of one half of IC neurons studied were correlated with the stimulus duty cycle. These neurons may preferentially process terminal phase information when the bat's pulse emission duty cycle increases. 6. While the stimulus RR affected the dynamic range and overall profile of the intensity rate function, only little effect was observed with different stimulus durations.     

Manifestations of dynamic coding of the amplitude-modulated sounds on the level of auditory nerve fibres

Average firing rate of the auditory nerve fiber as function of the level of the tone with the frequency equal to characteristic frequency of the fibers, can be defined as an input-output characteristic. It is known that the steepening of the input-output characteristic of the real auditory nerve fiber is more, and the width is less than the spontaneous activity of the fiber. The latter characterizes fiber's ability to generate spikes, if the stimulus is absent. However it is known, that the real auditory nerve fibers with low spontaneous activity reproduce amplitude modulation of the signals much better, than the fibers with high spontaneous activity. From the results of simulation experiments, it follows that the dynamic properties of the auditory nerve fibers, providing fine tuning or adaptation of a fiber threshold under the stimulus level but not the static input-output characteristics, are the reason of fibers reproduction of stimuli amplitude modulations. However the auditory nerve fibers with high spontaneous activity due to abrupt input-output characteristic are capable to reproduce modulations of sounds whose levels are lower than a threshold of the fiber, if a weak signal adds to a weak broadband noise. This is a phenomenon of stochastic resonance found in the reactions of auditory nerve fibers.