Responses to Social Vocalizations in the Inferior Colliculus of the Mustached Bat Are Influenced by Secondary Tuning Curves

2007 ◽  
Vol 98 (6) ◽  
pp. 3461-3472 ◽  
Author(s):  
Lars Holmstrom ◽  
Patrick D. Roberts ◽  
Christine V. Portfors
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Extended Model ◽  
Complex Frequency ◽  
Neural Responses ◽  
Tone Frequency ◽  
Tuning Curves ◽  
Mustached Bat ◽  
Dual Functions

Neurons in the inferior colliculus (IC) of the mustached bat integrate input from multiple frequency bands in a complex fashion. These neurons are important for encoding the bat's echolocation and social vocalizations. The purpose of this study was to quantify the contribution of complex frequency interactions on the responses of IC neurons to social vocalizations. Neural responses to single tones, two-tone pairs, and social vocalizations were recorded in the IC of the mustached bat. Three types of data driven stimulus-response models were designed for each neuron from single tone and tone pair stimuli to predict the responses of individual neurons to social vocalizations. The first model was generated only using the neuron's primary frequency tuning curve, whereas the second model incorporated the entire hearing range of the animal. The extended model often predicted responses to many social vocalizations more accurately for multiply tuned neurons. One class of multiply tuned neuron that likely encodes echolocation information also responded to many of the social vocalizations, suggesting that some neurons in the mustached bat IC have dual functions. The third model included two-tone frequency tunings of the neurons. The responses to vocalizations were better predicted by the two-tone models when the neuron had inhibitory frequency tuning curves that were not near the neuron's primary tuning curve. Our results suggest that complex frequency interactions in the IC determine neural responses to social vocalizations and some neurons in IC have dual functions that encode both echolocation and social vocalization signals.

Corticofugal Shaping of Frequency Tuning Curves in the Central Nucleus of the Inferior Colliculus of Mice

2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Primary Auditory Cortex ◽  
Nerve Fibers ◽  
Cortical Activation ◽  
Central Nucleus ◽  
Tuning Curves

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.

scholarly journals Multiple sounds degrade the frequency representation in monkey inferior colliculus

2020 ◽  
Author(s):  
Shawn M. Willett ◽  
Jennifer M. Groh
Keyword(s):  
Maximum Likelihood ◽  
Firing Rate ◽  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Response Functions ◽  
Tuning Curves ◽  
Frequency Representation ◽  
Simultaneous Sounds ◽  
Alternative Theories

AbstractHow we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One hypothesis is that tuning curves might change to limit the number of stimuli driving any given neuron when multiple stimuli are present. To test this hypothesis, we recorded the activity of neurons in the inferior colliculus while monkeys localized either one or two simultaneous sounds differing in frequency. Although monkeys easily distinguished simultaneous sounds (∼90% correct performance), the frequency tuning of inferior colliculus neurons on dual sound trials did not improve in any obvious way. Frequency selectivity was degraded on dual sound trials compared to single sound trials: tuning curves broadened, and frequency accounted for less of the variance in firing rate. These tuning curve changes led a maximum-likelihood decoder to perform worse on dual sound trials than on single sound trials. These results fail to support the hypothesis that changes in frequency response functions serve to reduce the overlap in the representation of simultaneous sounds. Instead these results suggest alternative theories, such as recent evidence of alternations in firing rate between the rates corresponding to each of the two stimuli, offer a more promising approach.

Sharpening of Frequency Tuning by Inhibition in the Thalamic Auditory Nucleus of the Mustached Bat

1997 ◽  
Vol 77 (4) ◽  
pp. 2098-2114 ◽  
Author(s):  
Nobuo Suga ◽  
Yunfeng Zhang ◽  
Jun Yan
Keyword(s):  
Frequency Tuning ◽  
Slow Component ◽  
Tuning Curve ◽  
Primary Auditory Cortex ◽  
Constant Frequency ◽  
Tuning Curves ◽  
Peripheral Neurons ◽  
Mustached Bat ◽  
Medial Geniculate ◽  
Auditory Nucleus

Suga, N., Y. Zhang, and J. Yan. Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. J. Neurophysiol. 77: 2098–2114, 1997. Unlike the quasitriangular frequency-tuning curves of peripheral neurons, pencil- or spindle-shaped frequency-tuning curves (excitatory areas) have been found in the central auditory systems of many species of animals belonging to different classes. Inhibitory tuning curves (areas) are commonly found on both sides of such “level-tolerant” sharp frequency-tuning curves. However, it has not yet been examined whether sharpening of frequency tuning takes place in the medial geniculate body (MGB). We injected an inhibitory transmitter antagonist, bicuculline methiodide (BMI), into the MGB of the mustached bat to examine whether frequency tuning is sharpened by inhibition in the MGB and whether this sharpening, if any, occurs in addition to that performed in prethalamic auditory nuclei. Thirty-seven percent of thalamic Doppler-shifted constant frequency (DSCF) neurons mostly showing a level-tolerant frequency-tuning curve had an inhibitory area or areas. BMI changed the inhibitory areas of these neurons into excitatory areas, so that their excitatory frequency-tuning curves became broader. However, the BMI-broadened excitatory frequency-tuning curves were still much narrower than those of peripheral neurons. Our results indicate that level-tolerant frequency tuning of thalamic DSCF neurons is mostly created by prethalamic auditory nuclei and that it is further sharpened in 37% of thalamic DSCF neurons by lateral inhibition occurring in the MGB. The comparisons in sharpness (quality factors) of frequency-tuning curves between peripheral, thalamic, and cortical DSCF neurons indicate that the skirt portion of tuning curves is sharper in the above order, and that their tip portion is not significantly different between the peripheral and thalamic DSCF neurons, but significantly sharper in the cortical DSCF neurons than in the thalamic DSCF neurons. Therefore the central auditory system has inhibitory mechanisms for the progressive sharpening of frequency tuning. DSCF neurons in the primary auditory cortex were recently found to show facilitative responses to paired sounds. That is, they are combination sensitive. In the present studies, we found that thalamic DSCF neurons also showed facilitative responses to paired sounds. The responses of thalamic DSCF neurons to acoustic stimuli consisted of a slow and a fast component. BMI mainly increased the slow component and an excitatory transmitter antagonist, d-2-amino-5-phosphonovalerate mainly suppressed the slow component. Therefore the response pattern of these thalamic neurons is shaped by both γ-aminobutyric acid-mediated inhibition and N-methyl-d-aspartate-mediated facilitation.

GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus

1992 ◽  
Vol 68 (5) ◽  
pp. 1760-1774 ◽  
Author(s):  
L. Yang ◽  
G. D. Pollak ◽  
C. Resler
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Sound Level ◽  
Response Properties ◽  
Tuning Curves ◽  
Rate Level ◽  
Wide Range ◽  
Discharge Patterns ◽  
Threshold Tuning

1. The influence of bicuculline on the tuning curves of 65 neurons in the inferior colliculus of the mustache bat was investigated. Single units were recorded with multibarrel electrodes where one barrel contained bicuculline, an antagonist specific for gamma-amino-butyric acid (GABA)A receptors. Fifty-nine tuning curves were recorded from units that were sharply tuned to 60 kHz, the dominant frequency of the bat's orientation call, but six tuning curves were also recorded from units tuned to lower frequencies and whose tuning curves were broader than the 60 kHz cells. Tuning curves were constructed from peristimulus time (PST) histograms obtained over a wide range of frequency-intensity combinations. Thus tuning curves, PST histograms evoked by frequencies within the tuning curve, and rate-level functions at the best frequency were obtained before iontophoresis of bicuculline and compared with the tuning curves and response properties obtained during the administration of bicuculline. 2. Three general types of tuning curves were obtained: 1) open tuning curves that broadened on both the high- and low-frequency sides with increasing sound level; 2) level-tolerant tuning curves in which the width of the tuning curve remained uniformly narrow with increasing sound level; and 3) upper-threshold tuning curves, which did not discharge to high-intensity tone bursts at the best frequency, thereby creating closed or folded tuning curves. 3. One major finding is that GABAergic inhibition plays an important role in sharpening frequency tuning properties of many neurons in the mustache bat inferior colliculus. In response to blocking GABAergic inputs with bicuculline, the tuning curves broadened in 42% of the neurons that were sharply tuned to 60 kHz. The degree of change in most units varied with sound level: tuning curves were least affected, or not affected at all, within 10 dB of threshold and showed progressively greater changes at higher sound levels. These effects were seen in units that had open, level-tolerant, and upper-threshold tuning curves. 4. A second key result is that bicuculline affected rate-level functions and/or temporal discharge patterns in many units. Bicuculline transformed the rate-level functions of 13 cells that originally had nonmonotonic rate level functions, from strongly nonmonotonic into weakly nonmonotonic or monotonic functions. It also changed the temporal discharge patterns in 22 cells, and the changes were often frequency specific.(ABSTRACT TRUNCATED AT 400 WORDS)

Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat

1985 ◽  
Vol 53 (4) ◽  
pp. 1109-1145 ◽  
Author(s):  
N. Suga ◽  
K. Tsuzuki
Keyword(s):  
Auditory Cortex ◽  
Frequency Analysis ◽  
Frequency Tuning ◽  
Neural Basis ◽  
Single Tone ◽  
Tuning Curves ◽  
Mustached Bat ◽  
Essential Components ◽  
High Stimulus ◽  
Pulse Echo

For echolocation the mustached bat, Pteronotus parnellii, emits complex orientation sounds (pulses), each consisting of four harmonics with long constant-frequency components (CF1-4) followed by short frequency-modulated components (FM1-4). The CF signals are best suited for target detection and measurement of target velocity. The CF/CF area of the auditory cortex of this species contains neurons sensitive to pulse-echo pairs. These CF/CF combination-sensitive neurons extract velocity information from Doppler-shifted echoes. In this study we electrophysiologically investigated the frequency tuning of CF/CF neurons for excitation, facilitation, and inhibition. CF1/CF2 and CF1/CF3 combination-sensitive neurons responded poorly to individual signal elements in pulse-echo pairs but showed strong facilitation of responses to pulse-echo pairs. The essential components in the pairs were CF1 of the pulse and CF2 or CF3 of the echo. In 68% of CF/CF neurons, the frequency-tuning curves for facilitation were extremely sharp for CF2 or CF3 and were "level-tolerant" so that the bandwidths of the tuning curves were less than 5.0% of best frequencies even at high stimulus levels. Facilitative tuning curves for CF1 were level tolerant only in 6% of the neurons studied. CF/CF neurons were specialized for fine analysis of the frequency relationship between two CF sounds regardless of sound pressure levels. Some CF/CF neurons responded to single-tone stimuli. Frequency-tuning curves for excitation (responses to single-tone stimuli) were extremely sharp and level tolerant for CF2 or CF3 in 59% of CF1/CF2 neurons and 70% of CF1/CF3 neurons. Tuning to CF1 was level tolerant in only 9% of these neurons. Sharp level-tolerant tuning may be the neural basis for small difference limens in frequency at high stimulus levels. Sharp level-tolerant tuning curves were sandwiched between broad inhibitory areas. Best frequencies for inhibition were slightly higher or lower than the best frequencies for facilitation and excitation. We thus conclude that sharp level-tolerant tuning curves are produced by inhibition. The extent to which neural sharpening occurred differed among groups of neurons tuned to different frequencies. The more important the frequency analysis of a particular component in biosonar signals, the more pronounced the neural sharpening. This was in addition to the peripheral specialization for fine frequency analysis of that component. The difference in bandwidth or quality factor between the excitatory tuning curves of peripheral neurons and the facilitative and excitatory tuning curves of CF/CF neurons was larger at higher stimulus levels.(ABSTRACT TRUNCATED AT 400 WORDS)

Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat

1975 ◽  
Vol 38 (5) ◽  
pp. 1208-1216 ◽  
Author(s):  
L. M. Aitkin ◽  
D. R. Moore
Keyword(s):  
Inferior Colliculus ◽  
Tuning Curve ◽  
External Auditory Meatus ◽  
Auditory Pathway ◽  
Central Nucleus ◽  
Synaptic Density ◽  
Tonotopic Organization ◽  
Tuning Curves ◽  
Sharp Form ◽  
Cochlear Development

Tuning curves were measured for 65 units in the inferior colliculus of seven anesthetized kittens aged from 6 to 28 days. At 2 days of age the inferior colliculus was divisible into central, pericentral, and external nuclei. Evidence was found for broader tuning curves to occur in the pericentral nucleus compared with the central nucleus, as has been observed in the adult. The middle ear was filled with serous fluid to 6 days, while the external auditory meatus remained collapsed until 10 days. Central nucleus tuning curves in kittens were relatively flat with high thresholds. Best-frequency thresholds diminished from a mean of near 100 dB SPL at 6-11 days to near 50 dB in the adult. The marked drop in thresholds between days 22 and 21 led to the adoption of the sharp form of tuning curve common for adults. Tonotopic organization of the central nucleus was clear at day 11. Speculations were advanced about the dependence of central auditory maturations on cochlear development, axon myelination in the auditory pathway, and changes in synaptic density as a function of age.

scholarly journals Different Serotonin Receptor Agonists Have Distinct Effects on Sound-Evoked Responses in Inferior Colliculus

2006 ◽  
Vol 96 (5) ◽  
pp. 2177-2188 ◽  
Author(s):  
Laura M. Hurley
Keyword(s):  
Inferior Colliculus ◽  
Auditory Processing ◽  
Serotonin Receptors ◽  
Serotonin Receptor ◽  
Frequency Tuning ◽  
Receptor Subtypes ◽  
Tuning Curves ◽  
Wide Range ◽  
Selective Agonists ◽  
Auditory Nucleus

The neuromodulator serotonin has a complex set of effects on the auditory responses of neurons within the inferior colliculus (IC), a midbrain auditory nucleus that integrates a wide range of inputs from auditory and nonauditory sources. To determine whether activation of different types of serotonin receptors is a source of the variability in serotonergic effects, four selective agonists of serotonin receptors in the serotonin (5-HT) 1 and 5-HT2 families were iontophoretically applied to IC neurons, which were monitored for changes in their responses to auditory stimuli. Different agonists had different effects on neural responses. The 5-HT1A agonist had mixed facilitatory and depressive effects, whereas 5-HT1B and 5-HT2C agonists were both largely facilitatory. Different agonists changed threshold and frequency tuning in ways that reflected their effects on spike count. When pairs of agonists were applied sequentially to the same neurons, selective agonists sometimes affected neurons in ways that were similar to serotonin, but not to other selective agonists tested. Different agonists also differentially affected groups of neurons classified by the shapes of their frequency-tuning curves, with serotonin and the 5-HT1 receptors affecting proportionally more non-V-type neurons relative to the other agonists tested. In all, evidence suggests that the diversity of serotonin receptor subtypes in the IC is likely to account for at least some of the variability of the effects of serotonin and that receptor subtypes fulfill specialized roles in auditory processing.

Tuning to Interaural Time Difference and Frequency Differs Between the Auditory Arcopallium and the External Nucleus of the Inferior Colliculus

2009 ◽  
Vol 101 (5) ◽  
pp. 2348-2361 ◽  
Author(s):  
Katrin Vonderschen ◽  
Hermann Wagner
Keyword(s):  
Inferior Colliculus ◽  
Tuning Curve ◽  
Interaural Time Difference ◽  
Low Frequency ◽  
Steep Slope ◽  
Time Difference ◽  
Interaural Time Differences ◽  
Tuning Curves ◽  
Barn Owls ◽  
Zero Time

Barn owls process sound-localization information in two parallel pathways, the midbrain and the forebrain pathway. Exctracellular recordings of neural responses to auditory stimuli from far advanced stations of these pathways, the auditory arcopallium in the forebrain and the external nucleus of the inferior colliculus in the midbrain, demonstrated that the representations of interaural time difference and frequency in the forebrain pathway differ from those in the midbrain pathway. Specifically, low-frequency representation was conserved in the forebrain pathway, while it was lost in the midbrain pathway. Variation of interaural time difference yielded symmetrical tuning curves in the midbrain pathway. By contrast, the typical forebrain-tuning curve was asymmetric with a steep slope crossing zero time difference and a less-steep slope toward larger contralateral time disparities. Low sound frequencies contributed sensitivity to contralateral leading sounds underlying these asymmetries, whereas high frequencies enhanced the steepness of slopes at small interaural time differences. Furthermore, the peaks of time-disparity tuning curves were wider in the forebrain than in the midbrain. The distribution of the steepest slopes of best interaural time differences in the auditory arcopallium, but not in the external nucleus of the inferior colliculus, was centered at zero time difference. The distribution observed in the auditory arocpallium is reminiscent of the situation observed in small mammals. We speculate that the forebrain representation may serve as a population code supporting fine discrimination of central interaural time differences and coarse indication of laterality of a stimulus for large interaural time differences.

Spatial map of frequency tuning-curve shapes in the mouse inferior colliculus

Neuroreport ◽  
2003 ◽  
Vol 14 (10) ◽  
pp. 1365-1369 ◽  
Author(s):  
Günter Ehret ◽  
Marina Egorova ◽  
Steffen R. Hage ◽  
Birgit A. Müller
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Tuning Curve

A Bayesian approach for characterizing direction tuning curves in the supplementary motor area of behaving monkeys

2013 ◽  
Vol 109 (11) ◽  
pp. 2842-2851 ◽  
Author(s):  
Hadas Taubman ◽  
Eilon Vaadia ◽  
Rony Paz ◽  
Gal Chechik
Keyword(s):  
Supplementary Motor Area ◽  
Tuning Curve ◽  
Motor Area ◽  
Movement Direction ◽  
Neural Responses ◽  
Shape Estimation ◽  
Tuning Curves ◽  
Coarse Resolution ◽  
Behaving Monkeys ◽  
Direction Tuning

Neural responses are commonly studied in terms of “tuning curves,” characterizing changes in neuronal response as a function of a continuous stimulus parameter. In the motor system, neural responses to movement direction often follow a bell-shaped tuning curve for which the exact shape determines the properties of neuronal movement coding. Estimating the shape of that tuning curve robustly is hard, especially when directions are sampled unevenly and at a coarse resolution. Here, we describe a Bayesian estimation procedure that improves the accuracy of curve-shape estimation even when the curve is sampled unevenly and at a very coarse resolution. Using this approach, we characterize the movement direction tuning curves in the supplementary motor area (SMA) of behaving monkeys. We compare the SMA tuning curves to tuning curves of neurons from the primary motor cortex (M1) of the same monkeys, showing that the tuning curves of the SMA neurons tend to be narrower and shallower. We also show that these characteristics do not depend on the specific location in each region.

Sign in / Sign up

Export Citation Format

Share Document