scholarly journals Organization and trade-off of spectro-temporal tuning properties of duration-tuned neurons in the mammalian inferior colliculus

2014 ◽  
Vol 111 (10) ◽  
pp. 2047-2060 ◽  
Author(s):  
James A. Morrison ◽  
Faranak Farzan ◽  
Thane Fremouw ◽  
Riziq Sayegh ◽  
Ellen Covey ◽  
...  
Keyword(s):  
Inferior Colliculus ◽  
Spatial Organization ◽  
Frequency Tuning ◽  
Stimulus Frequency ◽  
Neural Mechanism ◽  
Auditory Pathway ◽  
Complex Signal ◽  
Trade Off ◽  
Tuning Curves ◽  
Engineering Theory

Neurons throughout the mammalian central auditory pathway respond selectively to stimulus frequency and amplitude, and some are also selective for stimulus duration. First found in the auditory midbrain or inferior colliculus (IC), these duration-tuned neurons (DTNs) provide a potential neural mechanism for encoding temporal features of sound. In this study, we investigated how having an additional neural response filter, one selective to the duration of an auditory stimulus, influences frequency tuning and neural organization by recording single-unit responses and measuring the dorsal-ventral position and spectral-temporal tuning properties of auditory DTNs from the IC of the awake big brown bat ( Eptesicus fuscus). Like other IC neurons, DTNs were tonotopically organized and had either V-shaped, U-shaped, or O-shaped frequency tuning curves (excitatory frequency response areas). We hypothesized there would be an interaction between frequency and duration tuning in DTNs, as electrical engineering theory for resonant filters dictates a trade-off in spectral-temporal resolution: sharp tuning in the frequency domain results in poorer resolution in the time domain and vice versa. While the IC is a more complex signal analyzer than an electrical filter, a similar operational trade-off could exist in the responses of DTNs. Our data revealed two patterns of spectro-temporal sensitivity and spatial organization within the IC: DTNs with sharp frequency tuning and broad duration tuning were located in the dorsal IC, whereas cells with wide spectral tuning and narrow temporal tuning were found in the ventral IC.

scholarly journals Tonotopic and non-auditory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Aaron Benson Wong ◽  
J Gerard G Borst
Keyword(s):  
Inferior Colliculus ◽  
Spatial Organization ◽  
Functional Organization ◽  
Frequency Tuning ◽  
Gabaergic Neurons ◽  
Two Photon ◽  
Spontaneous Movements ◽  
Multimodal Information ◽  
Auditory Organization

The dorsal (DCIC) and lateral cortices (LCIC) of the inferior colliculus are major targets of the auditory and non-auditory cortical areas, suggesting a role in complex multimodal information processing. However, relatively little is known about their functional organization. We utilized in vivo two-photon Ca2+ imaging in awake mice expressing GCaMP6s in GABAergic or non-GABAergic neurons in the IC to investigate their spatial organization. We found different classes of temporal responses, which we confirmed with simultaneous juxtacellular electrophysiology. Both GABAergic and non-GABAergic neurons showed spatial microheterogeneity in their temporal responses. In contrast, a robust, double rostromedial-caudolateral gradient of frequency tuning was conserved between the two groups, and even among the subclasses. This, together with the existence of a subset of neurons sensitive to spontaneous movements, provides functional evidence for redefining the border between DCIC and LCIC.

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.

scholarly journals Neural population encoding and decoding of sound source location across sound level in the rabbit inferior colliculus

2016 ◽  
Vol 115 (1) ◽  
pp. 193-207 ◽  
Author(s):  
Mitchell L. Day ◽  
Bertrand Delgutte
Keyword(s):  
Inferior Colliculus ◽  
Sound Source ◽  
Auditory Pathway ◽  
Relevant Information ◽  
Sound Level ◽  
Neural Population ◽  
Linear Transformations ◽  
Tuning Curves ◽  
Azimuthal Position ◽  
Sound Levels

At lower levels of sensory processing, the representation of a stimulus feature in the response of a neural population can vary in complex ways across different stimulus intensities, potentially changing the amount of feature-relevant information in the response. How higher-level neural circuits could implement feature decoding computations that compensate for these intensity-dependent variations remains unclear. Here we focused on neurons in the inferior colliculus (IC) of unanesthetized rabbits, whose firing rates are sensitive to both the azimuthal position of a sound source and its sound level. We found that the azimuth tuning curves of an IC neuron at different sound levels tend to be linear transformations of each other. These transformations could either increase or decrease the mutual information between source azimuth and spike count with increasing level for individual neurons, yet population azimuthal information remained constant across the absolute sound levels tested (35, 50, and 65 dB SPL), as inferred from the performance of a maximum-likelihood neural population decoder. We harnessed evidence of level-dependent linear transformations to reduce the number of free parameters in the creation of an accurate cross-level population decoder of azimuth. Interestingly, this decoder predicts monotonic azimuth tuning curves, broadly sensitive to contralateral azimuths, in neurons at higher levels in the auditory pathway.

scholarly journals Tonotopic and multisensory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

2019 ◽  
Author(s):  
Aaron B. Wong ◽  
J. Gerard G. Borst
Keyword(s):  
Inferior Colliculus ◽  
Spatial Organization ◽  
Functional Organization ◽  
Frequency Tuning ◽  
Gabaergic Neurons ◽  
Temporal Response ◽  
Two Photon ◽  
Spontaneous Movements ◽  
Multimodal Information

AbstractThe dorsal (DCIC) and lateral cortices (LCIC) of the inferior colliculus are major targets of the auditory and non-auditory cortical areas, suggesting a role in complex multimodal information processing. However, relatively little is known about their functional organization. We utilized in vivo two-photon Ca2+ imaging in awake mice expressing GCaMP6s in GABAergic or non-GABAergic neurons in the IC to investigate their spatial organization. We found different classes of temporal response, which we confirmed with simultaneous juxtacellular electrophysiology. Both GABAergic and non-GABAergic neurons showed spatial microheterogeneity in their temporal responses. In contrast, a robust reversed rostromedial-caudolateral gradient of frequency tuning was conserved between the two groups, and even among the subclasses. This, together with the existence of a subset of neurons sensitive to spontaneous movements, provides functional evidence for redefining the border between DCIC and LCIC.

Length and width tuning of neurons in the cat's primary visual cortex

1994 ◽  
Vol 71 (1) ◽  
pp. 347-374 ◽  
Author(s):  
G. C. DeAngelis ◽  
R. D. Freeman ◽  
I. Ohzawa
Keyword(s):  
Receptive Field ◽  
Spatial Frequency ◽  
Spatial Organization ◽  
Striate Cortex ◽  
Frequency Tuning ◽  
Variable Parameter ◽  
Visual Space ◽  
Similar Degree ◽  
Tuning Curves ◽  
Number Of Cycles

1. The classically defined receptive field of a visual neuron is the area of visual space over which the cell responds to visual stimuli. It is well established, however, that the discharge produced by an optimal stimulus can be modulated by the presence of additional stimuli that by themselves do not produce any response. This study examines inhibitory influences that originate from areas located outside of the classical (i.e., excitatory) receptive field. Previous work has shown that for some cells the response to a properly oriented bar of light becomes attenuated when the bar extends beyond the receptive field, a phenomenon known as end-inhibition (or length tuning). Analogously, it has been shown that increasing the number of cycles of a drifting grating stimulus may also inhibit the firing of some cells, an effect known as side-inhibition (or width tuning). Very little information is available, however, about the relationship between end- and side-inhibition. We have examined the spatial organization and tuning characteristics of these inhibitory effects by recording extracellularly from single neurons in the cat's striate cortex (Area 17). 2. For each cortical neuron, length and width tuning curves were obtained with the use of rectangular patches of drifting sinusoidal gratings that have variable length and width. Results from 82 cells show that the strengths of end- and side-inhibition tend to be correlated. Most cells that exhibit clear end-inhibition also show a similar degree of side-inhibition. For these cells, the excitatory receptive field is surrounded on all sides by inhibitory zones. Some cells exhibit only end- or side-inhibition, but not both. Data for 28 binocular cells show that length and width tuning curves for the dominant and nondominant eyes tend to be closely matched. 3. We also measured tuning characteristics of end- and side-inhibition. To obtain these data, the excitatory receptive field was stimulated with a grating patch having optimal orientation, spatial frequency, and size, whereas the end- or side-inhibitory regions were stimulated with patches of gratings that had a variable parameter (such as orientation). Results show that end- and side-inhibition tend to be strongest at the orientation and spatial frequency that yield maximal excitation. However, orientation and spatial frequency tuning curves for inhibition are considerably broader than those for excitation, suggesting that inhibition is mediated by a pool of neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Comparison of Midbrain and Thalamic Space-Specific Neurons in Barn Owls

2006 ◽  
Vol 95 (2) ◽  
pp. 783-790 ◽  
Author(s):  
María Lucía Pérez ◽  
José Luis Peña
Keyword(s):  
Inferior Colliculus ◽  
Spatial Information ◽  
Receptive Fields ◽  
Stimulus Frequency ◽  
Auditory Pathway ◽  
Mammalian Brain ◽  
Neural Pathways ◽  
Spatial Cues ◽  
Auditory Space ◽  
Barn Owls

Spatial receptive fields of neurons in the auditory pathway of the barn owl result from the sensitivity to combinations of interaural time (ITD) and level differences across stimulus frequency. Both the forebrain and tectum of the owl contain such neurons. The neural pathways, which lead to the forebrain and tectal representations of auditory space, separate before the midbrain map of auditory space is synthesized. The first nuclei that belong exclusively to either the forebrain or the tectal pathways are the nucleus ovoidalis (Ov) and the external nucleus of the inferior colliculus (ICx), respectively. Both receive projections from the lateral shell subdivision of the inferior colliculus but are not interconnected. Previous studies indicate that the owl's tectal representation of auditory space is different from those found in the owl's forebrain and the mammalian brain. We addressed the question of whether the computation of spatial cues in both pathways is the same by comparing the ITD tuning of Ov and ICx neurons. Unlike in ICx, the relationship between frequency and ITD tuning had not been studied in single Ov units. In contrast to the conspicuous frequency independent ITD tuning of space-specific neurons of ICx, ITD selectivity varied with frequency in Ov. We also observed that the spatially tuned neurons of Ov respond to lower frequencies and are more broadly tuned to ITD than in ICx. Thus there are differences in the integration of frequency and ITD in the two sound-localization pathways. Thalamic neurons integrate spatial information not only within a broader frequency band but also across ITD channels.

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 Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

2017 ◽  
Vol 117 (4) ◽  
pp. 1636-1656 ◽  
Author(s):  
Roberto Valdizón-Rodríguez ◽  
Paul A. Faure
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Stimulus Frequency ◽  
Onset Time ◽  
Extracellular Recording ◽  
Tone Frequency ◽  
Unit Recording ◽  
Synaptic Inputs ◽  
Big Brown Bat ◽  
Paired Tone

Inhibition plays an important role in creating the temporal response properties of duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC). Neurophysiological and computational studies indicate that duration selectivity in the IC is created through the convergence of excitatory and inhibitory synaptic inputs offset in time. We used paired-tone stimulation and extracellular recording to measure the frequency tuning of the inhibition acting on DTNs in the IC of the big brown bat ( Eptesicus fuscus). We stimulated DTNs with pairs of tones differing in duration, onset time, and frequency. The onset time of a short, best-duration (BD), probe tone set to the best excitatory frequency (BEF) was varied relative to the onset of a longer-duration, nonexcitatory (NE) tone whose frequency was varied. When the NE tone frequency was near or within the cell’s excitatory bandwidth (eBW), BD tone-evoked spikes were suppressed by an onset-evoked inhibition. The onset of the spike suppression was independent of stimulus frequency, but both the offset and duration of the suppression decreased as the NE tone frequency departed from the BEF. We measured the inhibitory frequency response area, best inhibitory frequency (BIF), and inhibitory bandwidth (iBW) of each cell. We found that the BIF closely matched the BEF, but the iBW was broader and usually overlapped the eBW measured from the same cell. These data suggest that temporal selectivity of midbrain DTNs is created and preserved by having cells receive an onset-evoked, constant-latency, broadband inhibition that largely overlaps the cell’s excitatory receptive field. We conclude by discussing possible neural sources of the inhibition. NEW & NOTEWORTHY Duration-tuned neurons (DTNs) arise from temporally offset excitatory and inhibitory synaptic inputs. We used single-unit recording and paired-tone stimulation to measure the spectral tuning of the inhibitory inputs to DTNs. The onset of inhibition was independent of stimulus frequency; the offset and duration of inhibition systematically decreased as the stimulus departed from the cell’s best excitatory frequency. Best inhibitory frequencies matched best excitatory frequencies; however, inhibitory bandwidths were more broadly tuned than excitatory bandwidths.

Sign in / Sign up

Export Citation Format

Share Document