A Neuronal Correlate of the Precedence Effect Is Associated With Spatial Selectivity in the Barn Owl's Auditory Midbrain

2004 ◽  
Vol 92 (4) ◽  
pp. 2051-2070 ◽  
Author(s):  
Matthew W. Spitzer ◽  
Avinash D. S. Bala ◽  
Terry T. Takahashi

Sound localization in echoic conditions depends on a precedence effect (PE), in which the first arriving sound dominates the perceived location of later reflections. Previous studies have demonstrated neurophysiological correlates of the PE in several species, but the underlying mechanisms remain unknown. The present study documents responses of space-specific neurons in the barn owl's inferior colliculus (IC) to stimuli simulating direct sounds and reflections that overlap in time at the listener's ears. Responses to 100-ms noises with lead-lag delays from 1 to 100 ms were recorded from neurons in the space-mapped subdivisions of IC in anesthetized owls (N2O/isofluorane). Responses to a target located at a unit's best location were usually suppressed by a masker located outside the excitatory portion of the spatial receptive field. The least spatially selective units exhibited temporally symmetric effects, in that the amount of suppression was the same whether the masker led or lagged. Such effects mirror the alteration of localization cues caused by acoustic superposition of leading and lagging sounds. In more spatially selective units, the suppression was often temporally asymmetric, being more pronounced when the masker led. The masker often evoked small changes in spatial tuning that were not related to the magnitude of suppressive effects. The association of temporally asymmetric suppression with spatial selectivity suggests that this property emerges within IC, and not at earlier stages of auditory processing. Asymmetric suppression reduces the ability of highly spatially selective neurons to encode the location of lagging sounds, providing a possible basis for the PE.

2004 ◽  
Vol 92 (6) ◽  
pp. 3286-3297 ◽  
Author(s):  
Daniel J. Tollin ◽  
Luis C. Populin ◽  
Tom C. T. Yin

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.


2015 ◽  
Vol 114 (5) ◽  
pp. 2991-3001 ◽  
Author(s):  
Andrew D. Brown ◽  
Heath G. Jones ◽  
Alan Kan ◽  
Tanvi Thakkar ◽  
G. Christopher Stecker ◽  
...  

Normal-hearing human listeners and a variety of studied animal species localize sound sources accurately in reverberant environments by responding to the directional cues carried by the first-arriving sound rather than spurious cues carried by later-arriving reflections, which are not perceived discretely. This phenomenon is known as the precedence effect (PE) in sound localization. Despite decades of study, the biological basis of the PE remains unclear. Though the PE was once widely attributed to central processes such as synaptic inhibition in the auditory midbrain, a more recent hypothesis holds that the PE may arise essentially as a by-product of normal cochlear function. Here we evaluated the PE in a unique human patient population with demonstrated sensitivity to binaural information but without functional cochleae. Users of bilateral cochlear implants (CIs) were tested in a psychophysical task that assessed the number and location(s) of auditory images perceived for simulated source-echo (lead-lag) stimuli. A parallel experiment was conducted in a group of normal-hearing (NH) listeners. Key findings were as follows: 1) Subjects in both groups exhibited lead-lag fusion. 2) Fusion was marginally weaker in CI users than in NH listeners but could be augmented by systematically attenuating the amplitude of the lag stimulus to coarsely simulate adaptation observed in acoustically stimulated auditory nerve fibers. 3) Dominance of the lead in localization varied substantially among both NH and CI subjects but was evident in both groups. Taken together, data suggest that aspects of the PE can be elicited in CI users, who lack functional cochleae, thus suggesting that neural mechanisms are sufficient to produce the PE.


2020 ◽  
Vol 123 (5) ◽  
pp. 1791-1807 ◽  
Author(s):  
Ryan Dorkoski ◽  
Kenneth E. Hancock ◽  
Gareth A. Whaley ◽  
Timothy R. Wohl ◽  
Noelle C. Stroud ◽  
...  

A “division of labor” has previously been assumed in which the directions of low- and high-frequency sound sources are thought to be encoded by neurons preferentially sensitive to low and high frequencies, respectively. Contrary to this, we found that auditory midbrain neurons encode the directions of both low- and high-frequency sounds regardless of their preferred frequencies. Neural responses were shaped by different sound localization cues depending on the stimulus spectrum—even within the same neuron.


2021 ◽  
Vol 15 ◽  
Author(s):  
Arianna Gentile Polese ◽  
Sunny Nigam ◽  
Laura M. Hurley

Neuromodulatory systems may provide information on social context to auditory brain regions, but relatively few studies have assessed the effects of neuromodulation on auditory responses to acoustic social signals. To address this issue, we measured the influence of the serotonergic system on the responses of neurons in a mouse auditory midbrain nucleus, the inferior colliculus (IC), to vocal signals. Broadband vocalizations (BBVs) are human-audible signals produced by mice in distress as well as by female mice in opposite-sex interactions. The production of BBVs is context-dependent in that they are produced both at early stages of interactions as females physically reject males and at later stages as males mount females. Serotonin in the IC of males corresponds to these events, and is elevated more in males that experience less female rejection. We measured the responses of single IC neurons to five recorded examples of BBVs in anesthetized mice. We then locally activated the 5-HT1A receptor through iontophoretic application of 8-OH-DPAT. IC neurons showed little selectivity for different BBVs, but spike trains were characterized by local regions of high spike probability, which we called “response features.” Response features varied across neurons and also across calls for individual neurons, ranging from 1 to 7 response features for responses of single neurons to single calls. 8-OH-DPAT suppressed spikes and also reduced the numbers of response features. The weakest response features were the most likely to disappear, suggestive of an “iceberg”-like effect in which activation of the 5-HT1A receptor suppressed weakly suprathreshold response features below the spiking threshold. Because serotonin in the IC is more likely to be elevated for mounting-associated BBVs than for rejection-associated BBVs, these effects of the 5-HT1A receptor could contribute to the differential auditory processing of BBVs in different behavioral subcontexts.


Author(s):  
Adrian Rees ◽  
Llwyd D. Orton

Commissural fibres interconnecting the two sides of the brain are found at several points along the auditory pathway, thus suggesting their fundamental importance for the analysis of sound. This chapter presents an overview of what is currently known about the anatomy, physiology, and behavioral influences of the commissure of the inferior colliculus (CoIC)—the most prominent brainstem auditory commissure—that reciprocally interconnects the principal nuclei of the auditory midbrain, the inferior colliculi (IC). The primary contribution to the CoIC originates from neurons projecting from one inferior colliculus to the other, with the dorsal cortex and central nucleus providing the most extensive connections. In addition, many ascending and descending auditory centers send projections to the IC via the CoIC, together with diverse sources located outside the classically defined auditory pathway. The degree of interconnection between the two ICs suggests they function as a single entity. Recent in vivo evidence has established that CoIC projections modulate the neural representation of sound frequency, level, and location in the IC, thus indicating an important role for the CoIC in auditory processing. However, there is limited evidence for the influence of the CoIC on auditory behavior. This, together with the diversity of sources projecting via the CoIC, suggest unknown roles that warrant further exploration.


Author(s):  
Laura Hurley

The inferior colliculus (IC) receives prominent projections from centralized neuromodulatory systems. These systems include extra-auditory clusters of cholinergic, dopaminergic, noradrenergic, and serotonergic neurons. Although these modulatory sites are not explicitly part of the auditory system, they receive projections from primary auditory regions and are responsive to acoustic stimuli. This bidirectional influence suggests the existence of auditory-modulatory feedback loops. A characteristic of neuromodulatory centers is that they integrate inputs from anatomically widespread and functionally diverse sets of brain regions. This connectivity gives neuromodulatory systems the potential to import information into the auditory system on situational variables that accompany acoustic stimuli, such as context, internal state, or experience. Once released, neuromodulators functionally reconfigure auditory circuitry through a variety of receptors expressed by auditory neurons. In addition to shaping ascending auditory information, neuromodulation within the IC influences behaviors that arise subcortically, such as prepulse inhibition of the startle response. Neuromodulatory systems therefore provide a route for integrative behavioral information to access auditory processing from its earliest levels.


2020 ◽  
Vol 123 (6) ◽  
pp. 2101-2121 ◽  
Author(s):  
Anna O. Nguyen ◽  
Devin K. Binder ◽  
Iryna M. Ethell ◽  
Khaleel A. Razak

Autism spectrum disorders (ASD) are commonly associated with sensory sensitivity issues, but the underlying mechanisms are unclear. This study presents novel evidence for neural correlates of auditory hypersensitivity in the developing inferior colliculus (IC) in the Fmr1 knockout (KO) mouse, a mouse model of Fragile X Syndrome (FXS), a leading genetic cause of ASD. Responses begin to show genotype differences between postnatal days 14 and 21, suggesting an early developmental treatment window.


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