scholarly journals Information conveyed by inferior colliculus neurons about stimuli with aligned and misaligned sound localization cues

2011 ◽  
Vol 106 (2) ◽  
pp. 974-985 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Virtual Space ◽  
Central Nucleus ◽  
Single Neurons ◽  
Interaural Time Differences ◽  
Marmoset Monkey ◽  
Interaural Level Differences ◽  
Broadband Sound ◽  
Response Area

Previous studies have demonstrated that single neurons in the central nucleus of the inferior colliculus (ICC) are sensitive to multiple sound localization cues. We investigated the hypothesis that ICC neurons are specialized to encode multiple sound localization cues that are aligned in space (as would naturally occur from a single broadband sound source). Sound localization cues including interaural time differences (ITDs), interaural level differences (ILDs), and spectral shapes (SSs) were measured in a marmoset monkey. Virtual space methods were used to generate stimuli with aligned and misaligned combinations of cues while recording in the ICC of the same monkey. Mutual information (MI) between spike rates and stimuli for aligned versus misaligned cues were compared. Neurons with best frequencies (BFs) less than ∼11 kHz mostly encoded information about a single sound localization cue, ITD or ILD depending on frequency, consistent with the dominance of ear acoustics by either ITD or ILD at those frequencies. Most neurons with BFs >11 kHz encoded information about multiple sound localization cues, usually ILD and SS, and were sensitive to their alignment. In some neurons MI between stimuli and spike responses was greater for aligned cues, while in others it was greater for misaligned cues. If SS cues were shifted to lower frequencies in the virtual space stimuli, a similar result was found for neurons with BFs <11 kHz, showing that the cue interaction reflects the spectra of the stimuli and not a specialization for representing SS cues. In general the results show that ICC neurons are sensitive to multiple localization cues if they are simultaneously present in the frequency response area of the neuron. However, the representation is diffuse in that there is not a specialization in the ICC for encoding aligned sound localization cues.

Cues for Sound Localization Are Encoded in Multiple Aspects of Spike Trains in the Inferior Colliculus

2008 ◽  
Vol 99 (4) ◽  
pp. 1672-1682 ◽  
Author(s):  
Steven M. Chase ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Discharge Rate ◽  
Spike Timing ◽  
Virtual Space ◽  
Dependent Manner ◽  
Single Neurons ◽  
Information Theoretic ◽  
Independent Information ◽  
Interaural Level Differences ◽  
Spike Latency

To localize sound, information from three cues—interaural timing differences (ITDs), interaural level differences (ILDs), and spectral notch cues (SNs)—must be properly integrated. The inferior colliculus (IC) receives convergent input from neurons encoding all three cues. Using virtual space stimuli and information theoretic techniques, we investigated the coding of the various localization cues in single neurons of the IC under different encoding schemes. Here we focus on the analysis of information encoded by first-spike latency, in comparison to previous results on discharge rate and ongoing spike timing. The results show that the localization cues converge to different degrees in particular neurons. ITD information is conveyed most strongly by spike rate, with small amounts of independent information in latency and ongoing spike timing. ILD information shows a similar pattern, with larger mutual information values for all three cues. For these cues, ongoing spike timing does not typically contribute independent information over that captured by a joint rate/first-spike latency code. SNs are coded by both rate and first-spike latency, but ongoing spike timing significantly enhances their representation in a best frequency–dependent manner, as long as the temporal envelope of the stimulus can be used in the decoder. The differential coding of the localization cues suggests that information about multiple cues could be multiplexed onto the responses of single neurons.

Single-Unit Responses in the Inferior Colliculus of Decerebrate Cats II. Sensitivity to Interaural Level Differences

1999 ◽  
Vol 82 (1) ◽  
pp. 164-175 ◽  
Author(s):  
Kevin A. Davis ◽  
Ramnarayan Ramachandran ◽  
Bradford J. May
Keyword(s):  
Frequency Response ◽  
Inferior Colliculus ◽  
Free Field ◽  
Central Nucleus ◽  
Type I ◽  
Discharge Rates ◽  
Ipsilateral Stimulation ◽  
Interaural Level Differences ◽  
Type V ◽  
Decerebrate Cats

Single units in the central nucleus of the inferior colliculus (ICC) of unanesthetized decerebrate cats can be grouped into three distinct types (V, I, and O) according to the patterns of excitation and inhibition revealed in contralateral frequency response maps. This study extends the description of these response types by assessing their ipsilateral and binaural response map properties. Here the nature of ipsilateral inputs is evaluated directly using frequency response maps and compared with results obtained from methods that rely on sensitivity to interaural level differences (ILDs). In general, there is a one-to-one correspondence between observed ipsilateral input characteristics and those inferred from ILD manipulations. Type V units receive ipsilateral excitation and show binaural facilitation (EE properties); type I and type O units receive ipsilateral inhibition and show binaural excitatory/inhibitory (EI) interactions. Analyses of binaural frequency response maps show that these ILD effects extend over the entire receptive field of ICC units. Thus the range of frequencies that elicits excitation from type V units is expanded with increasing levels of ipsilateral stimulation, whereas the excitatory bandwidth of type I and O units decreases under the same binaural conditions. For the majority of ICC units, application of bicuculline, an antagonist for GABAA-mediated inhibition, does not alter the basic effects of binaural stimulation; rather, it primarily increases spontaneous and maximum discharge rates. These results support our previous interpretations of the putative dominant inputs to ICC response types and have important implications for midbrain processing of competing free-field sounds that reach the listener with different directional signatures.

scholarly journals Evidence of a Functionally Segregated Pathway from Lateral Superior Olive to Inferior Colliculus

2019 ◽  
Author(s):  
Nathaniel T. Greene ◽  
Kevin A. Davis
Keyword(s):  
Inferior Colliculus ◽  
Excitatory Amino Acid ◽  
Excitatory Input ◽  
Central Nucleus ◽  
Type I ◽  
Lateral Superior Olive ◽  
Reversible Inactivation ◽  
Superior Olive ◽  
Receptive Field Organization ◽  
Interaural Level Differences

ABSTRACTNeurons in the central nucleus of the inferior colliculus (ICC) of decerebrate cats show three major response patterns when tones of different frequencies and levels are presented to the contralateral ear. The frequency response maps of type I units uniquely exhibit a narrowly tuned I-shaped area of excitation around best frequency (the most sensitive frequency) and flanking regions of inhibition at lower and higher frequencies. Type I units receive ipsilateral inhibition, and show binaural excitatory/inhibitory interactions. Lateral superior olive (LSO) principal cells display a similar receptive field organization and sensitivity to interaural level differences (ILDs) and project directly to the ICC, therefore are supposed to be the dominant source of excitatory input for type I units. To test this hypothesis, the responses of ICC units were compared before and after reversible inactivation of the LSO by injection of the non-specific excitatory amino-acid antagonist kynurenic acid. When excitatory activity within the LSO was blocked, many ICC type I units (~50%) were silenced or showed substantially decreased activitycomparable. By contrast, the responses of the other two ICC unit types were largely unaffected. With regard to the origins of unaffected ICC type I units, evidence indicates that the LSO was inactivated in an incomplete, anisotropic manner, and the monaural and binaural responses of such units are similar to those of affected type I units. Taken together, these results support the interpretation that most type I units are the midbrain components of a functionally segregated ILD processing pathway initiated by the LSO.

Neural Correlates of the Precedence Effect in the Inferior Colliculus of Behaving Cats

2004 ◽  
Vol 92 (6) ◽  
pp. 3286-3297 ◽  
Author(s):  
Daniel J. Tollin ◽  
Luis C. Populin ◽  
Tom C. T. Yin
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Species Differences ◽  
Behavioral Responses ◽  
Neural Correlates ◽  
Precedence Effect ◽  
Single Neurons ◽  
Localization Dominance ◽  
Echo Threshold ◽  
Spatial Locations

Several auditory spatial illusions, collectively called the precedence effect (PE), occur when transient sounds are presented from two different spatial locations but separated in time by an interstimulus delay (ISD). For ISDs in the range of localization dominance (<10 ms), a single fused sound is typically located near the leading source location only, as if the location of the lagging source were suppressed. For longer ISDs, both the leading and lagging sources can be heard and localized, and the shortest ISD where this occurs is called the echo threshold. Previous physiological studies of the extracellular responses of single neurons in the inferior colliculus (IC) of anesthetized cats and unanesthetized rabbits with sounds known to elicit the PE have shown correlates of these phenomena though there were differences in the physiologically measured echo thresholds. Here we recorded in the IC of awake, behaving cats using stimuli that we have shown to evoke behavioral responses that are consistent with the precedence effect. For small ISDs, responses to the lag were reduced or eliminated consistent with psychophysical data showing that sound localization is based on the leading source. At longer ISDs, the responses to the lagging source recovered at ISDs comparable to psychophysically measured echo thresholds. Thus it appears that anesthesia, and not species differences, accounts for the discrepancies in the earlier studies.

scholarly journals Inferior colliculus syndrome: Clinical magnetic resonance microscopy anatomic analysis on a 7 T system

2017 ◽  
Vol 5 ◽  
pp. 2050313X1774520
Author(s):  
Ingrid L Kwee ◽  
Hitoshi Matsuzawa ◽  
Kazunori Nakada ◽  
Yukihiko Fujii ◽  
Tsutomu Nakada
Keyword(s):  
Hearing Loss ◽  
Magnetic Resonance ◽  
Inferior Colliculus ◽  
Sound Localization ◽  
Imaging System ◽  
Central Nucleus ◽  
Magnetic Resonance Microscopy ◽  
Magnetic Resonance Imaging System ◽  
The Right ◽  
T System

We performed detailed structural analysis of a case of a unilateral lesion of the inferior colliculus using magnetic resonance microscopy on a 7 T system. A 36-year-old right-handed man had an intracerebral hemorrhage circumscribed to the right inferior colliculus. Following recovery from the acute phase, he had only residual left ear tinnitus and left trochlear palsy and no hearing loss. Microscopic imaging analysis on a 7 T magnetic resonance imaging system demonstrated a chronic lesion confined primarily to the right central nucleus of the inferior colliculus. Sound localization was significantly impaired in the contralateral hemispace. The case confirms prior clinical reports of unilateral inferior colliculus dysfunction, the specific anatomic characterization of which was demonstrated in this case by magnetic resonance microscopy. It furthermore supports the notion that central nucleus of the inferior colliculus dysfunction can produce tinnitus and sound localization deficits, without hearing loss

scholarly journals Alignment of sound localization cues in the nucleus of the brachium of the inferior colliculus

2014 ◽  
Vol 111 (12) ◽  
pp. 2624-2633 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Additive Model ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Auditory Space ◽  
Directional Filtering ◽  
Spectral Cues ◽  
Spatial Alignment ◽  
Auditory Space Map

Accurate sound localization is based on three acoustic cues (interaural time and intensity difference and spectral cues from directional filtering by the pinna). In natural listening conditions, every spatial position of a sound source provides a unique combination of these three cues in “natural alignment.” Although neurons in the central nucleus (ICC) of the inferior colliculus (IC) are sensitive to multiple cues, they do not favor their natural spatial alignment. We tested for sensitivity to cue alignment in the nucleus of the brachium of the IC (BIN) in unanesthetized marmoset monkeys. The BIN receives its predominant auditory input from ICC and projects to the topographic auditory space map in the superior colliculus. Sound localization cues measured in each monkey were used to synthesize broadband stimuli with aligned and misaligned cues; spike responses to these stimuli were recorded in the BIN. We computed mutual information (MI) between the set of spike rates and the stimuli containing either aligned or misaligned cues. The results can be summarized as follows: 1) BIN neurons encode more information about auditory space when cues are aligned compared with misaligned. 2) Significantly more units prefer aligned cues in the BIN than in ICC. 3) An additive model based on summing the responses to stimuli with the localization cues varying individually accurately predicts the alignment preference with all cues varying. Overall, the results suggest that the BIN is the first site in the ascending mammalian auditory system that is tuned to natural combinations of sound localization cues.

scholarly journals Dual sensitivity of inferior colliculus neurons to ITD in the envelopes of high-frequency sounds: experimental and modeling study

2014 ◽  
Vol 111 (1) ◽  
pp. 164-181 ◽  
Author(s):  
Le Wang ◽  
Sasha Devore ◽  
Bertrand Delgutte ◽  
H. Steven Colburn
Keyword(s):  
Simple Model ◽  
Computational Model ◽  
Inferior Colliculus ◽  
Sound Localization ◽  
High Frequency ◽  
Modulation Frequency ◽  
Primary Site ◽  
Interaural Time Differences ◽  
Binaural Interaction ◽  
Unanesthetized Rabbit

Human listeners are sensitive to interaural time differences (ITDs) in the envelopes of sounds, which can serve as a cue for sound localization. Many high-frequency neurons in the mammalian inferior colliculus (IC) are sensitive to envelope-ITDs of sinusoidally amplitude-modulated (SAM) sounds. Typically, envelope-ITD-sensitive IC neurons exhibit either peak-type sensitivity, discharging maximally at the same delay across frequencies, or trough-type sensitivity, discharging minimally at the same delay across frequencies, consistent with responses observed at the primary site of binaural interaction in the medial and lateral superior olives (MSO and LSO), respectively. However, some high-frequency IC neurons exhibit dual types of envelope-ITD sensitivity in their responses to SAM tones, that is, they exhibit peak-type sensitivity at some modulation frequencies and trough-type sensitivity at other frequencies. Here we show that high-frequency IC neurons in the unanesthetized rabbit can also exhibit dual types of envelope-ITD sensitivity in their responses to SAM noise. Such complex responses to SAM stimuli could be achieved by convergent inputs from MSO and LSO onto single IC neurons. We test this hypothesis by implementing a physiologically explicit, computational model of the binaural pathway. Specifically, we examined envelope-ITD sensitivity of a simple model IC neuron that receives convergent inputs from MSO and LSO model neurons. We show that dual envelope-ITD sensitivity emerges in the IC when convergent MSO and LSO inputs are differentially tuned for modulation frequency.

Serotonin Effects on Frequency Tuning of Inferior Colliculus Neurons

2001 ◽  
Vol 85 (2) ◽  
pp. 828-842 ◽  
Author(s):  
Laura M. Hurley ◽  
George D. Pollak
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Gain Control ◽  
Central Nucleus ◽  
Complex Signals ◽  
Constant Intensity ◽  
Fm Signals ◽  
Spectral Components ◽  
Induced Changes ◽  
Response Area

We investigated the modulatory effects of serotonin on the tuning of 114 neurons in the central nucleus of the inferior colliculus (ICc) of Mexican free-tailed bats and how serotonin-induced changes in tuning influenced responses to complex signals. We obtained a “response area” for each neuron, defined as the frequency range that evoked discharges and the spike counts evoked by those frequencies at a constant intensity. We then iontophoretically applied serotonin and compared response areas obtained before and during the application of serotonin. In 58 cells, we also assessed how serotonin-induced changes in response areas correlated with changes in the responses to brief frequency-modulated (FM) sweeps whose structure simulated natural echolocation calls. Serotonin profoundly changed tone-evoked spike counts in 60% of the neurons (68/114). In most neurons, serotonin exerted a gain control, facilitating or depressing the responses to all frequencies in their response areas. In many cells, serotonergic effects on tones were reflected in the responses to FM signals. The most interesting effects were in those cells in which serotonin selectively changed the responsiveness to only some frequencies in the neuron's response area and had little or no effect on other frequencies. This caused predictable changes in responses to the more complex FM sweeps whose spectral components passed through the neurons' response areas. Our results suggest that serotonin, whose release varies with behavioral state, functionally reconfigures the circuitry of the IC and may modulate the perception of acoustic signals under different behavioral states.

scholarly journals Forebrain Pathway for Auditory Space Processing in the Barn Owl

1998 ◽  
Vol 79 (2) ◽  
pp. 891-902 ◽  
Author(s):  
Yale E. Cohen ◽  
Greg L. Miller ◽  
Eric I. Knudsen
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Spatial Information ◽  
Barn Owl ◽  
Afferent Input ◽  
Central Nucleus ◽  
Appreciable Effect ◽  
Auditory Space ◽  
Space Processing ◽  
Field L

Cohen, Yale E., Greg L. Miller, and Eric I. Knudsen. Forebrain pathway for auditory space processing in the barn owl. J. Neurophysiol. 79: 891–902, 1998. The forebrain plays an important role in many aspects of sound localization behavior. Yet, the forebrain pathway that processes auditory spatial information is not known for any species. Using standard anatomic labeling techniques, we used a “top-down” approach to trace the flow of auditory spatial information from an output area of the forebrain sound localization pathway (the auditory archistriatum, AAr), back through the forebrain, and into the auditory midbrain. Previous work has demonstrated that AAr units are specialized for auditory space processing. The results presented here show that the AAr receives afferent input from Field L both directly and indirectly via the caudolateral neostriatum. Afferent input to Field L originates mainly in the auditory thalamus, nucleus ovoidalis, which, in turn, receives input from the central nucleus of the inferior colliculus. In addition, we confirmed previously reported projections of the AAr to the basal ganglia, the external nucleus of the inferior colliculus (ICX), the deep layers of the optic tectum, and various brain stem nuclei. A series of inactivation experiments demonstrated that the sharp tuning of AAr sites for binaural spatial cues depends on Field L input but not on input from the auditory space map in the midbrain ICX: pharmacological inactivation of Field L eliminated completelyauditory responses in the AAr, whereas bilateral ablation of the midbrain ICX had no appreciable effect on AAr responses. We conclude, therefore, that the forebrain sound localization pathway can process auditory spatial information independently of the midbrain localization pathway.

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