Ambiguities in Sound-Duration Selectivity by Neurons in the Inferior Colliculus of the Bat Molossus molossus From Cuba

2004 ◽  
Vol 91 (5) ◽  
pp. 2215-2226 ◽  
Author(s):  
Emanuel C. Mora ◽  
Manfred Kössl
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure ◽  
Pressure Level ◽  
Auditory Neurons ◽  
Echolocation Calls ◽  
Band Pass ◽  
Molossus Molossus ◽  
Species Specific ◽  
Filter Mechanism ◽  
Sound Duration

This study examines duration selectivity in auditory neurons of the inferior colliculus of the bat Molossus molossus (Molossidae, Chiroptera) from Cuba. Three main types of duration selectivity, short-, band-, and long-pass, as previously described in other species, are present in M. molossus. The range of best durations in the inferior colliculus of this species approximates the durations of their echolocation calls, suggesting that, as has been shown in other species of bats and frogs, the filter mechanism that produces duration tuning is selective for species-specific sounds relevant to behavior. Duration coding in M. molossus is not unambiguous because ∼30% of the short- and band-pass neurons respond best to two different stimulus durations. This bimodal duration selectivity could be explained by time delayed excitatory inputs that coincide with an inhibitory rebound. In addition, the effect of stimulus intensity on duration selectivity was tested. For most of the neurons (78%), duration selectivity was affected by absolute sound pressure level and/or small changes of sound pressure. In this respect, the processing of stimulus duration by collicular neurons seems to be more complex in M. molossus than in other species studied so far.

Duration Selective Neurons in the Inferior Colliculus of the Rat: Topographic Distribution and Relation of Duration Sensitivity to Other Response Properties

2006 ◽  
Vol 95 (2) ◽  
pp. 823-836 ◽  
Author(s):  
D. Pérez-González ◽  
M. S. Malmierca ◽  
J. M. Moore ◽  
O. Hernández ◽  
E. Covey
Keyword(s):  
Inferior Colliculus ◽  
Excitatory Input ◽  
Central Nucleus ◽  
Response Patterns ◽  
Dorsal Cortex ◽  
Auditory Midbrain ◽  
Duration Threshold ◽  
Band Pass ◽  
Species Specific ◽  
Sound Duration

Many animals use duration to help them identify the source and meaning of a sound. Duration-sensitive neurons have been found in the auditory midbrain of mammals and amphibians, where their selectivity seems to correspond to the lengths of species-specific vocalizations. In this study, single neurons in the rat inferior colliculus (IC) were tested for sensitivity to sound duration. About one-half (54%) of the units sampled showed some form of duration selectivity. The majority of these (76%) were long-pass neurons that responded to sounds exceeding some duration threshold (range: 5–60 ms). Band-pass neurons, which only responded to a restricted range of durations, made up 13% of duration-sensitive neurons (best durations: 15–120 ms). Other units displayed short-pass (2%) or mixed (9%) response patterns. The majority of duration-sensitive neurons were localized outside the central nucleus of the IC, especially in the dorsal cortex, where more than one-half of the neurons sampled had long-pass selectivity for duration. Band-pass duration tuned neurons were only found outside the central nucleus. Characteristics of duration-sensitive neurons in the rat support the idea that this filtering arises through an interaction of excitatory and inhibitory inputs that converge in the IC. Band-pass neurons typically responded at sound offset, suggesting that their tuning is created through the same mechanisms that have been described in echolocating bats. The finding that the first-spike latencies of all long-pass neurons were longer than the shortest duration to which they responded supports the idea that they receive transient inhibition before, or simultaneously with, a sustained excitatory input. The ranges of selectivity in rat IC neurons are within the range of durations of rat vocalizations. These data suggest that a population of neurons in the rat IC have evolved to transmit information about behaviorally relevant sound durations using mechanisms that are common to all mammals, with an emphasis on long-pass tuning characteristics.

Response Selectivity for Species-Specific Calls in the Inferior Colliculus of Mexican Free-Tailed Bats is Generated by Inhibition

2002 ◽  
Vol 88 (4) ◽  
pp. 1941-1954 ◽  
Author(s):  
Achim Klug ◽  
Eric E. Bauer ◽  
Joshua T. Hanson ◽  
Laura Hurley ◽  
John Meitzen ◽  
...  
Keyword(s):  
Inferior Colliculus ◽  
Social Communication ◽  
Predictive Accuracy ◽  
Tone Burst ◽  
Spatiotemporal Pattern ◽  
Population Response ◽  
Excitatory Response ◽  
Echolocation Calls ◽  
Discharge Patterns ◽  
Species Specific

Here we show that inhibition shapes diverse responses to species-specific calls in the inferior colliculus (IC) of Mexican free-tailed bats. We presented 10 calls to each neuron of which 8 were social communication and 2 were echolocation calls. We also measured excitatory response regions: the range of tone burst frequencies that evoked discharges at a fixed intensity. The calls evoked highly selective responses in that IC neurons responded to some calls but not others even though those calls swept through their excitatory response regions. By convolving activity in the response regions with the spectrogram of each call, we evaluated whether responses to tone bursts could predict discharge patterns evoked by species-specific calls. The convolutions often predicted responses to calls that evoked no responses and thus were inaccurate. Blocking inhibition at the IC reduced or eliminated selectivity and greatly improved the predictive accuracy of the convolutions. By comparing the responses evoked by two calls with similar spectra, we show that each call evoked a unique spatiotemporal pattern of activity distributed across and within isofrequency contours and that the disparity in the population response was greatly reduced by blocking inhibition. Thus the inhibition evoked by each call can shape a unique pattern of activity in the IC population and that pattern may be important for both the identification of a particular call and for discriminating it from other calls and other signals.

Duration tuning in the inferior colliculus of the mustached bat

2011 ◽  
Vol 106 (6) ◽  
pp. 3119-3128 ◽  
Author(s):  
Silvio Macías ◽  
Emanuel C. Mora ◽  
Julio C. Hechavarría ◽  
Manfred Kössl
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure ◽  
Frequency Range ◽  
Constant Frequency ◽  
Third Harmonic ◽  
Mustached Bat ◽  
Pteronotus Parnellii ◽  
Sound Levels ◽  
Response Profile ◽  
Band Pass

We studied duration tuning in neurons of the inferior colliculus (IC) of the mustached bat. Duration-tuned neurons in the IC of the mustached bat fall into three main types: short (16 of 136), band (34 of 136), and long (29 of 136) pass. The remaining 51 neurons showed no selectivity for the duration of sounds. The distribution of best durations was double peaked with maxima around 3 and 17 ms, which correlate with the duration of the short frequency-modulated (FM) and the long constant-frequency (CF) signals emitted by Pteronotus parnellii. Since there are no individual neurons with a double-peaked duration response profile, both types of temporal processing seem to be well segregated in the IC. Most short- and band-pass units with best frequency in the CF2 range responded to best durations > 9 ms (66%, 18 of 27 units). However, there is no evidence for a bias toward longer durations as there is for neurons tuned to the frequency range of the FM component of the third harmonic, where 83% (10 of 12 neurons) showed best durations longer than 9 ms. In most duration-tuned neurons, response areas as a function of stimulus duration and intensity showed either V or U shape, with duration tuning retained across the range of sound levels tested. Duration tuning was affected by changes in sound pressure level in only six neurons. In all duration-tuned neurons, latencies measured at the best duration were longer than best durations, suggesting that behavioral decisions based on analysis of the duration of the pulses would not be expected to be complete until well after the stimulus has occurred.

Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences

1990 ◽  
Vol 63 (3) ◽  
pp. 570-591 ◽  
Author(s):  
D. R. Irvine ◽  
G. Gago
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure Level ◽  
High Frequency ◽  
Sound Pressure ◽  
Pressure Level ◽  
Central Nucleus ◽  
Sensitivity Functions ◽  
Rate Intensity ◽  
Ipsilateral Stimulation ◽  
Intensity Functions

1. Development of models of the manner in which interaural intensity differences (IIDs), the major binaural cue for the azimuthal location of high-frequency sounds, are coded by populations of neurons requires knowledge of the extent to which the IID sensitivity of individual neurons is invariant with changes in sound pressure level (SPL) and other stimulus parameters. To examine this tissue, recordings were obtained from a large sample (n = 458) of neurons with characteristic frequency (CF) greater than 3 kHz in the central nucleus of the inferior colliculus (ICC) of anesthetized cats. The sensitivity to IIDs and the effects of changes in SPL on this sensitivity were examined in neurons receiving excitatory contralateral input and inhibitory or mixed inhibitory/facilitatory ipsilateral input (EI neurons). 2. The form of an EI neuron's IID sensitivity and the effects of changes in SPL on that sensitivity were found to be determined in part by the characteristics of the neuron's rate-intensity function for monaural contralateral stimulation, and detailed rate-intensity functions were therefore obtained for 91 neurons. Many ICC neurons have nonmonotonic rate-intensity functions, the proportion so classified depending on the criterion of nonmonotonicity employed. 3. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for 90 neurons, using a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range in which a function was obtained for each unit, the majority of EI neurons (72%) had monotonic (sigmoidal) or near-monotonic IID sensitivity functions. The remainder had nonmonotonic (peaked) IID sensitivity functions, which were attributable either to mixed inhibitory and facilitatory ipsilateral influences or to the fact that the effects of ipsilateral stimulation were superimposed on nonmonotonic effects of changes in intensity at the excitatory ear. 4. IID sensitivity was examined at two or more ABIs (3-5 in most cases) for 40 neurons classified as having monotonic or near-monotonic functions in the standard ABI range and for 7 neurons classified as nonmonotonic. For a small proportion of neurons with monotonic IID sensitivity functions, the form of the function was relatively invariant with changes in ABI. In those monotonic neurons in which the form of the IID sensitivity function varied with changes in ABI, the most common type of variation was that the position of the sloping portion of the function shifted systematically in the direction of larger IIDs favoring the ipsilateral ear as ABI increased.(ABSTRACT TRUNCATED AT 400 WORDS)

Echolocation calls produced by Trachops cirrhosus (Chiroptera: Phyllostomatidae) while hunting for frogs

1981 ◽  
Vol 59 (5) ◽  
pp. 750-753 ◽  
Author(s):  
R. M. R. Barclay ◽  
M. B. Fenton ◽  
M. D. Tuttle ◽  
M. J. Ryan
Keyword(s):  
Sound Pressure Level ◽  
Sound Pressure ◽  
Pressure Level ◽  
Echolocation Calls ◽  
Low Intensity ◽  
Flight Cage ◽  
Trachops Cirrhosus

The echolocation calls produced by Trachops cirrhosus in the field and in a flight cage were recorded as they hunted for frogs. The calls were of low intensity (< 70 dB sound pressure level (SPL) at 10 cm), short (less than 1 ms), multiharmonic frequency modulated sweeps with energy from over 100 to around 50 kHz. During most successful attacks of frogs in the cage, these orientation sounds were produced by the bats which are also known to rely on frog calls to locate prey.

Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences

1993 ◽  
Vol 69 (2) ◽  
pp. 449-461 ◽  
Author(s):  
M. N. Semple ◽  
L. M. Kitzes
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Sound Pressure Level ◽  
Sound Pressure ◽  
Primary Auditory Cortex ◽  
Response Strength ◽  
Simple Relation ◽  
Pressure Level ◽  
Interaural Level Difference ◽  
Single Neurons

1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (> 90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in > 60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural Measurement of Sound Duration: Control by Excitatory-Inhibitory Interactions in the Inferior Colliculus

2000 ◽  
Vol 84 (3) ◽  
pp. 1475-1487 ◽  
Author(s):  
John H. Casseday ◽  
Daphna Ehrlich ◽  
Ellen Covey
Keyword(s):  
Inferior Colliculus ◽  
Narrow Range ◽  
Auditory Pathway ◽  
Big Brown Bat ◽  
Before And After ◽  
Band Pass ◽  
Sound Duration ◽  
Onset Response ◽  
Inhibitory Interactions ◽  
Peak Value

In the inferior colliculus (IC) of the big brown bat, a subpopulation of cells (∼35%) are tuned to a narrow range of sound durations. Band-pass tuning for sound duration has not been seen at lower levels of the auditory pathway. Previous work suggests that it arises at the IC through the interaction of sound-evoked, temporally offset, excitatory and inhibitory inputs. To test this hypothesis, we recorded from duration-tuned neurons in the IC and examined duration tuning before and after iontophoretic infusion of antagonists to γ-aminobutyric acid-A (GABAA) (bicuculline) or glycine (strychnine). The criterion for duration tuning was that the neuron's spike count as a function of duration had a peak value at one duration or a range of durations that was ≥2 times the lowest nonzero value at longer durations. Out of 21 units tested with bicuculline, duration tuning was eliminated in 15, broadened in two, and unaltered in four. Out of 10 units tested with strychnine, duration tuning was eliminated in four, broadened in one, and unaltered in five. For units tested with both bicuculline and strychnine, bicuculline had a greater effect on reducing or abolishing duration tuning than did strychnine. Bicuculline and strychnine both produced changes in discharge pattern. There was nearly always a shift from an offset response to an onset response, indicating that in the predrug condition, inhibition arrived simultaneously with excitation or preceded it. There was often an increase in the length of the spike train, indicating that in the predrug condition, inhibition also coincided with later parts of excitation. These findings support two hypotheses. First, duration tuning is created in the IC. Second, although the construction of duration tuning varies in some details among IC neurons, it follows three rules: 1) an excitatory and an inhibitory event are temporally linked to the onset of sound but temporally offset from one another; 2) the duration of some inhibitory event must be linked to the duration of the sound; 3) an excitatory event must be linked to the offset of sound.

scholarly journals Effect of sound pressure level on contralateral inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

2019 ◽  
Vol 122 (1) ◽  
pp. 184-202
Author(s):  
Roberto Valdizón-Rodríguez ◽  
Dominika Kovaleva ◽  
Paul A. Faure
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure Level ◽  
Time Course ◽  
Sound Pressure ◽  
Dynamic Range ◽  
Onset Time ◽  
Pressure Level ◽  
Half Maximum ◽  
Synaptic Inputs ◽  
Rate Level

Duration tuning in the mammalian inferior colliculus (IC) is created by the interaction of excitatory and inhibitory synaptic inputs. We used extracellular recordings and paired tone stimulation to measure the strength and time course of the contralateral inhibition underlying duration-tuned neurons (DTNs) in the IC of the awake bat. The onset time of a short, best duration (BD), excitatory probe tone set to +10 dB (re threshold) was varied relative to the onset of a longer-duration, nonexcitatory (NE) suppressor tone whose sound pressure level (SPL) was varied. Spikes evoked by the roving BD tone were suppressed when the stationary NE tone amplitude was at or above the BD tone threshold. When the NE tone was increased from 0 to +10 dB, the inhibitory latency became shorter than the excitatory first-spike latency and the duration of inhibition increased, but no further changes occurred at +20 dB (re BD tone threshold). We used the effective duration of inhibition as a function of the NE tone amplitude to obtain suppression-level functions that were used to estimate the inhibitory half-maximum SPL (ISPL50). We also measured rate-level functions of DTNs with single BD tones varied in SPL and modeled the excitatory half-maximum SPL (ESPL50). There was a correlation between the ESPL50 and ISPL50, and the dynamic range of excitation and inhibition were similar. We conclude that the strength of inhibition changes in proportion to excitation as a function of SPL, and this feature likely contributes to the amplitude tolerance of the responses of DTNs. NEW & NOTEWORTHY Duration-tuned neurons arise from excitatory and inhibitory synaptic inputs offset in time. We measured the strength and time course of inhibition to changes in sound level. The onset of inhibition shortened while its duration lengthened as the stimulus level increased from 0 to +10 dB re threshold; however, no further changes were observed at +20 dB. Excitatory rate-level and inhibitory suppression-level response functions were strongly correlated, suggesting a mechanism for level tolerance in duration tuning.

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