Sensitivity of high‐frequency inferior colliculus neurons to sinusoidal amplitude‐modulation of low‐frequency tones

1. Localization of sounds has traditionally been considered to be performed by a duplex mechanism utilizing interaural temporal differences (ITDs) at low frequencies and interaural intensity differences at higher frequencies. More recently, it has been found that listeners can detect ITDs at high frequencies if the amplitude of the sound varies and an ITD is present in the envelope. Here we report the responses of neurons in the inferior colliculi of unanesthetized rabbits to ITDs of the envelopes of sinusoidally amplitude-modulated (SAM) tones. 2. Neurons were studied extracellularly with glass-coated Pt-Ir or Pt-W microelectrodes. Their sensitivity to ITDs in the envelopes of high-frequency sounds (> or = 2 kHz) was assessed using SAM tones that were presented binaurally. The tones at the two ears had the same carrier frequency but modulation frequencies that differed by 1 Hz. This caused a cyclic variation in the ITD produced by the envelope. In this "binaural SAM" stimulus, the carriers caused no ITD because they were in phase. In addition to the binaural SAM stimulus, pure tones were used to investigate responses to ipsilateral and contralateral stimulation and the nature of the interaction during binaural stimulation. 3. Neurons tended to display one of two kinds of sensitivity to ITDs. Some neurons discharged maximally at the same ITD at all modulation frequencies > 250 Hz (peak-type neurons), whereas others were maximally suppressed at the same ITD (trough-type neurons). 4. At these higher modulation frequencies (> 250 Hz), the characteristic delays that neurons exhibited tended to lie within the range that a rabbit might normally encounter (+/- 300 microseconds). The peak-type neurons favored ipsilateral delays, which correspond to sounds in the contralateral sound field. The trough-type neurons showed no such preference. 5. The preference of peak-type neurons for a particular delay was sharper than that of trough-type neurons and was comparable to that observed in neurons of the inferior colliculus that are sensitive to delays of low-frequency pure tones. 6. At lower modulation frequencies (< 150 Hz) characteristic delays often lay beyond +/- 300 microseconds. 7. Increasing the ipsilateral intensity tended to shift the preferred delay ipsilaterally at lower (< 250 Hz), but not at higher, modulation frequencies. 8. When tested with pure tones, a substantial number of peak-type neurons were found to be excited by contralateral stimulation but inhibited by ipsilateral stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

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Off-channel effect of high-frequency overstimulation on duration tuning of low-frequency inferior colliculus neurons in guinea pigs

Acta Oto-Laryngologica ◽

10.3109/00016480902856562 ◽

2009 ◽

Vol 129 (12) ◽

pp. 1451-1455

Author(s):

Zhengnong Chen ◽

Dongzhen Yu ◽

Yanmei Feng ◽

Kaiming Su ◽

Jian Wang ◽

...

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Guinea Pigs ◽

Low Frequency ◽

Channel Effect

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Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1994.72.3.1061 ◽

1994 ◽

Vol 72 (3) ◽

pp. 1061-1079 ◽

Cited By ~ 89

Author(s):

Z. M. Fuzessery

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Low Frequency ◽

Central Nucleus ◽

Frequency Change ◽

Frequency Range ◽

Low Frequencies ◽

Response Properties ◽

Sweep Direction ◽

Pallid Bat

1. While hunting, the pallid bat uses passive sound localization at low frequencies to find terrestrial prey, and echolocation for general orientation. It must therefore process two different types of acoustic input at the same time. The pallid bat's echolocation pulse is a downward frequency-modulated (FM) sweep from 60 to 30 kHz. This study examined the response selectivity of single neurons in the pallid bat's central nucleus of the inferior colliculus (ICC) for FM sweeps, comparing the response properties of the high-frequency population, tuned to the biosonar pulse, with the low-frequency population, tuned below the pulse. The working hypothesis was that the high-frequency population would exhibit a response selectivity for downward FM sweeps that was not present in the low-frequency population. 2. Neurons were tested for their selectivity for FM sweep direction, duration, frequency range and bandwidth, and rate of frequency change. The extent to which they responded exclusively to tones, noise, and FM sweeps was also examined. Significant differences in the response properties of neurons in the two populations were found. In the low-frequency population, all neurons responded to tones, but only 50% responded to FM sweeps. Only 23% were selective for sweep direction. In the high-frequency population, all neurons responded to FM sweeps, but 31% did not respond to tones. Over one-half of this population was selective for sweep direction, and of those that were selective, all preferred the downward sweep direction of the biosonar pulse. A large percentage (31%) responded exclusively to downward sweeps, and not to tones or upward sweeps. None of the cells in either population responded to noise, or did so only at very high relative thresholds. 3. Both populations contained neurons that were selective for short stimulus durations that approximated the duration of the biosonar pulse, although the percentage was greater in the high-frequency population (58% vs. 20%). In the high-frequency population, 31% of the neurons tested for duration responded exclusively to both the sweep direction and duration of the biosonar pulse. 4. Downward FM-selective neurons, with one exception, were generally insensitive to the rate of frequency change of the FM sweep, as well as the frequency range and bandwidth of the sweep. They responded similarly to both the full 60- to 30-kHz sweep and to 5-kHz bandwidth portions of the full sweep.(ABSTRACT TRUNCATED AT 400 WORDS)

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Off-channel effect of high-frequency overstimulation on duration tuning of low-frequency inferior colliculus neurons in guinea pigs

Acta Oto-Laryngologica ◽

10.1080/00016480902856562 ◽

2009 ◽

pp. 1-5

Author(s):

Zhengnong Chen ◽

Dongzhen Yu ◽

Yanmei Feng ◽

Kaiming Su ◽

Jian Wang ◽

...

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Guinea Pigs ◽

Low Frequency ◽

Channel Effect

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Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Inferior Colliculus of the Pallid Bat

Journal of Neurophysiology ◽

10.1152/jn.00021.2006 ◽

2006 ◽

Vol 96 (3) ◽

pp. 1320-1336 ◽

Cited By ~ 46

Author(s):

Zoltan M. Fuzessery ◽

Marlin D. Richardson ◽

Michael S. Coburn

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Tuning Curve ◽

Low Frequency ◽

Shape Selectivity ◽

Similar Rate ◽

Central Nucleus ◽

Arrival Times ◽

Sweep Direction ◽

Pallid Bat

This study describes mechanisms that underlie neuronal selectivity for the direction and rate of frequency-modulated sweeps in the central nucleus of the inferior colliculus (ICC) of the pallid bat ( Antrozous pallidus). This ICC contains a high percentage of neurons (66%) that respond selectively to the downward sweep direction of the bat's echolocation pulse. Some (19%) are specialists that respond only to downward sweeps. Most neurons (83%) are also tuned to sweep rates. A two-tone inhibition paradigm was used to describe inhibitory mechanisms that shape selectivity for sweep direction and rate. Two different mechanisms can create similar rate tuning. The first is an early on-best frequency inhibition that shapes duration tuning, which in turn determines rate tuning. In most neurons that are not duration tuned, a delayed high-frequency inhibition creates rate tuning. These neurons respond to fast sweep rates, but are inhibited as rate slows, and delayed inhibition overlaps excitation. In these neurons, starting a downward sweep within the excitatory tuning curve eliminates rate tuning. However, if rate tuning is shaped by duration tuning, this manipulation has no effect. Selectivity for the downward sweep direction is created by an early low-frequency inhibition that prevents responses to upward sweeps. In addition to this asymmetry in arrival times of low- and high-frequency inhibitions, the bandwidth of the low-frequency sideband was broader. Bandwidth influences the arrival time of inhibition during an FM sweep because a broader sideband will be encountered sooner. These findings show that similar spectrotemporal filters can be created by different mechanisms.

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Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.90390.2008 ◽

2008 ◽

Vol 100 (2) ◽

pp. 629-645 ◽

Cited By ~ 23

Author(s):

Diana Coomes Peterson ◽

Sergiy Voytenko ◽

Donald Gans ◽

Alexander Galazyuk ◽

Jeffrey Wenstrup

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Low Frequency ◽

Intracellular Recordings ◽

Multiple Frequency ◽

Response Facilitation ◽

Vocal Signals ◽

Postinhibitory Rebound ◽

Auditory Systems ◽

Combinatorial Interactions

In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combination-sensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low- and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency–tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency–evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency–evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency–tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency–evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.

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Effects of aging, hearing loss, and anatomical location on thresholds of inferior colliculus neurons in C57BL/6 and CBA mice

Journal of Neurophysiology ◽

10.1152/jn.1986.56.2.391 ◽

1986 ◽

Vol 56 (2) ◽

pp. 391-408 ◽

Cited By ~ 153

Author(s):

J. F. Willott

Keyword(s):

Hearing Loss ◽

Inferior Colliculus ◽

High Frequency ◽

Low Frequency ◽

Mouse Strains ◽

Anatomical Location ◽

Cba Mice ◽

Age Related ◽

Second Year Of Life ◽

Second Year

Multiple-unit threshold curves (MTCs) were obtained from inferior colliculus (IC) neurons across much of the (approximately 2-2.5 yr) life-span of two inbred mouse strains: the C57BL/6, which undergoes progressive age-related sensorineural hearing loss; and the CBA, which maintains good sensitivity until well into the second year of life. Tonotopic organization (the orderly dorsoventral arrangement of frequency sensitivity) is disrupted in the IC central nucleus (ICC) of aging C57 mice. Dorsal (low-frequency) MTCs change little during the first year of life, but in more ventral (high-frequency) regions high-frequency portions of MTCs are eliminated, best frequencies become lower, and low-frequency thresholds are reduced. These changes make the curves more similar to one another along the dorsoventral axis. During the second year of life, all thresholds become greatly elevated with neurons throughout the IC responding only to middle frequencies at very high intensities. In C57 mice, Q10 ratios (a measure of MTC tip sharpness) decline after 7 mo. The decline of Q10 with aging is associated with the age-related lowering of best frequencies and elevation of thresholds, both of which are positively correlated with smaller Q10s. The frequency range of C57 MTCs begins to decrease at 14 mo of age, when hearing loss is quite severe at all frequencies. In CBA mice, the above changes are minimal or do not occur even in 22 mo olds, which have moderate loss of sensitivity across all frequencies. Even in young mice (prior to demonstrable cochlear pathology in C57 mice), there are differences in MTCs between the two strains employed, with sensitivity of CBA mice being "shifted" toward higher frequencies. Age-related changes in MTC properties depend on the pattern of hearing loss (e.g., high frequency vs. flat) and the dorsoventral location of neurons within the ICC.

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EPSP Amplitude Modulation at the Rat Ia-Alpha Motoneuron Synapse: Effects of GABAB Receptor Agonists and Antagonists

Journal of Neurophysiology ◽

10.1152/jn.1998.79.1.181 ◽

1998 ◽

Vol 79 (1) ◽

pp. 181-189 ◽

Cited By ~ 24

Author(s):

Kavita R. Peshori ◽

William F. Collins ◽

Lorne M. Mendell

Keyword(s):

Amplitude Modulation ◽

High Frequency ◽

Low Frequency ◽

High Frequency Stimulation ◽

Posttetanic Potentiation ◽

Epsp Amplitude ◽

Frequency Stimulation ◽

The Relationship ◽

Receptor Agonists And Antagonists ◽

Cgp 35348

Peshori, Kavita R., William F. Collins III, and Lorne M. Mendell. EPSP amplitude modulation at the rat Ia-alpha motoneuron synapse: effects of GABAB receptor agonists and antagonists. J. Neurophysiol. 79: 181–189, 1998. The object of this study was to examine the relationship between excitatory postsynaptic potential (EPSP) amplitude, posttetanic potentiation, and EPSP amplitude modulation at synapses made by group Ia afferents on motoneurons in the rat. These relationships were evaluated in cells in untreated rats and in cells in rats treated with the γ-aminobutyric acid-B (GABAB) receptor agonist baclofen and antagonist CGP-35348, which were used to manipulate Ca2+ entry into presynaptic terminals and consequently probability of transmitter release from them. There was no evidence for postsynaptic action of these drugs from measurement of their effects on motoneuron properties. During high-frequency stimulation (32 shock bursts at 167 Hz), EPSP amplitude either decreased (negative modulation) or increased (positive modulation) in response to successive stimuli at different connections. In untreated rats this frequency-dependent amplitude modulation behavior was inversely but weakly correlated with EPSP amplitude measured at low frequency. Intravenous (iv) administration of the GABAB agonist, baclofen, produced a marked and progressive decrease in EPSP amplitude measured at low frequency coincident with a change in frequency-dependent EPSP amplitude modulation toward more positive values (synaptic facilitation). In contrast, an increase in EPSP amplitude occurred after iv administration of the GABAB antagonist CGP-35348 that was accompanied by a negative shift in EPSP amplitude modulation during high-frequency stimulation. The negative shift in EPSP amplitude modulation (synaptic depression) after CGP-35348 application was much smaller than the positive shift induced by baclofen when normalized to the change in EPSP amplitude. Posttetanic potentiation decreased after baclofen but did not increase after CGP-35348. The relationship between modulation and EPSP amplitude was much steeper after GABAB receptor manipulation in either direction than that observed in the population of motoneurons in untreated preparations. This suggests that in the rat differences in probability of release play at most a small role in determining EPSP amplitude across the motoneuron pool.

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Amplitude Modulation Detection by Listeners with Unilateral Dead Regions

Journal of the American Academy of Audiology ◽

10.3766/jaaa.20.10.2 ◽

2009 ◽

Vol 20 (10) ◽

pp. 597-606

Author(s):

Brian C.J. Moore

Keyword(s):

Hearing Loss ◽

Amplitude Modulation ◽

High Frequency ◽

Hearing Level ◽

Detection Thresholds ◽

High Frequency Hearing Loss ◽

Frequency Components ◽

Noise Test ◽

The Dead ◽

Sinusoidal Amplitude Modulation

Background: A dead region is a region in the cochlea where the inner hair cells and/or neurons are functioning very poorly, if at all. We have shown that, for people with sensorineural hearing loss, thresholds for detecting sinusoidal amplitude modulation (AM) of a sinusoidal carrier were lower for ears with high-frequency dead regions, as diagnosed using the threshold-equalizing noise test, calibrated in hearing level, than for ears without dead regions when the carrier frequency was below the edge frequency, fe, of the dead region. Purpose: To measure AM-detection thresholds for subjects with unilateral dead regions, using carrier frequencies both below and above fe. Research Design: Ten subjects with bilateral high-frequency hearing loss, but with unilateral high-frequency dead regions, were tested. The carriers were presented at sensation levels of 5, 10, or 15 dB. The values of fe were close to 1000, 1500, or 2000 Hz. Results: For carrier frequencies below fe, AM-detection thresholds were lower for the ears with dead regions than for the ears without dead regions, replicating earlier findings. In contrast, for carrier frequencies above fe, AM-detection thresholds tended to be higher for ears with dead regions than for ears without dead regions. Conclusions: The reason why AM detection was poorer in the ears with dead regions for carrier frequencies above fe is unclear. However, this finding is consistent with the generally poor discrimination of sounds that has been reported previously for sounds with frequency components falling within a dead region. The results have implications for the ability of people with dead regions to use information from frequency components falling inside the dead region.

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