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Article ; Online: Intracellular recordings reveal integrative function of the basolateral amygdala in acoustic communication.

Voytenko, Sergiy / Shanbhag, Sharad / Wenstrup, Jeffrey / Galazyuk, Alexander

2023 Volume 129, Issue 6, Page(s) 1334–1343

Abstract: The amygdala, a brain center of emotional expression, contributes to appropriate behavior responses during acoustic communication. In support of that role, the basolateral amygdala (BLA) analyzes the meaning of vocalizations through the integration of ... ...

Abstract	The amygdala, a brain center of emotional expression, contributes to appropriate behavior responses during acoustic communication. In support of that role, the basolateral amygdala (BLA) analyzes the meaning of vocalizations through the integration of multiple acoustic inputs with information from other senses and an animal's internal state. The mechanisms underlying this integration are poorly understood. This study focuses on the integration of vocalization-related inputs to the BLA from auditory centers during this processing. We used intracellular recordings of BLA neurons in unanesthetized big brown bats that rely heavily on a complex vocal repertoire during social interactions. Postsynaptic and spiking responses of BLA neurons were recorded to three vocal sequences that are closely related to distinct behaviors (appeasement, low-level aggression, and high-level aggression) and have different emotional valence. Our novel findings are that most BLA neurons showed postsynaptic responses to one or more vocalizations (31 of 46) but that many fewer neurons showed spiking responses (8 of 46). The spiking responses were more selective than postsynaptic potential (PSP) responses. Furthermore, vocal stimuli associated with either positive or negative valence were similarly effective in eliciting excitatory postsynaptic potentials (EPSPs), inhibitory postsynaptic potentials (IPSPs), and spiking responses. This indicates that BLA neurons process both positive- and negative-valence vocal stimuli. The greater selectivity of spiking responses than PSP responses suggests an integrative role for processing within the BLA to enhance response specificity in acoustic communication.
MeSH term(s)	Animals ; Basolateral Nuclear Complex ; Neurons/physiology ; Amygdala/physiology ; Vocalization, Animal/physiology ; Acoustics
Language	English
Publishing date	2023-04-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00103.2023
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Article ; Online: The Mouse Inferior Colliculus Responds Preferentially to Non-Ultrasonic Vocalizations.

Tehrani, Mahtab / Shanbhag, Sharad / Huyck, Julia J / Patel, Rahi / Kazimierski, Diana / Wenstrup, Jeffrey J

eNeuro

2024 Volume 11, Issue 4

Abstract: The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multichannel recordings to characterize and localize ... ...

Abstract	The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multichannel recordings to characterize and localize responses to social vocalizations and synthetic stimuli within the IC of female and male mice, both urethane anesthetized and unanesthetized. We compared responses to ultrasonic vocalizations (USVs) with other vocalizations in the mouse repertoire and related vocal responses to frequency tuning, IC subdivisions, and sex. Responses to lower frequency, broadband social vocalizations were widespread in IC, well represented throughout the tonotopic axis, across subdivisions, and in both sexes. Responses to USVs were much more limited. Although we observed some differences in tonal and vocal responses by sex and subdivision, representations of vocal responses by sex and subdivision were largely the same. For most units, responses to vocal signals occurred only when frequency response areas overlapped with spectra of the vocal signals. Since tuning to frequencies contained within the highest frequency USVs is limited (<15% of IC units), responses to these vocalizations are correspondingly limited (<5% of sound-responsive units). These results highlight a paradox of USV processing in some rodents: although USVs are the most abundant social vocalization, their representation and the representation of corresponding frequencies are less than lower frequency social vocalizations. We interpret this paradox in light of observations suggesting that USVs with lower frequency elements (<50 kHz) are associated with increased emotional intensity and engage a larger population of neurons in the mouse auditory system.
MeSH term(s)	Mice ; Female ; Male ; Animals ; Inferior Colliculi/physiology ; Ultrasonics ; Vocalization, Animal/physiology ; Sound ; Mesencephalon
Language	English
Publishing date	2024-04-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0097-24.2024
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Article: The Mouse Inferior Colliculus Responds Preferentially to Non-Ultrasonic Vocalizations.

Tehrani, Mahtab / Shanbhag, Sharad / Huyck, Julia J / Patel, Rahi / Kazimiersky, Diana / Wenstrup, Jeffrey J

bioRxiv : the preprint server for biology

2024

Abstract: The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multi-channel recordings to characterize and localize ... ...

Abstract	The inferior colliculus (IC), the midbrain auditory integration center, analyzes information about social vocalizations and provides substrates for higher level processing of vocal signals. We used multi-channel recordings to characterize and localize responses to social vocalizations and synthetic stimuli within the IC of female and male mice, both urethane-anesthetized and unanesthetized. We compared responses to ultrasonic vocalizations (USVs) with other vocalizations in the mouse repertoire and related vocal responses to frequency tuning, IC subdivisions, and sex. Responses to lower frequency, broadband social vocalizations were widespread in IC, well represented throughout the tonotopic axis, across subdivisions, and in both sexes. Responses to USVs were much more limited. Although we observed some differences in tonal and vocal responses by sex and subdivision, representations of vocal responses by sex and subdivision were largely the same. For most units, responses to vocal signals occurred only when frequency response areas overlapped with spectra of the vocal signals. Since tuning to frequencies contained within the highest frequency USVs is limited (< 15% of IC units), responses to these vocalizations are correspondingly limited (< 5% of sound-responsive units). These results highlight a paradox of USV processing in some rodents: although USVs are the most abundant social vocalization, their representation and the representation of corresponding frequencies is less than lower frequency social vocalizations. We interpret this paradox in light of observations suggesting that USVs with lower frequency elements (<50 kHz) are associated with increased emotional intensity and engage a larger population of neurons in the mouse auditory system. Significance statement: The inferior colliculus (IC) integrates multiple inputs to analyze information about social vocalizations. In mice, we show that the most common type of social vocalization, the ultrasonic vocalization or USV, was poorly represented in IC compared to lower frequency vocalizations. For most neurons, responses to vocal signals occurred only when frequency response areas overlapped with vocalization spectra. These results highlight a paradox of USV processing in some rodent auditory systems: although USVs are the most abundant social vocalization, their representation and representation of corresponding frequencies is less than lower frequency social vocalizations. These results suggest that USVs with lower frequency elements (<50 kHz)-associated with increased emotional intensity-will engage a larger population of neurons in the mouse auditory system.
Language	English
Publishing date	2024-02-11
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.09.579664
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Article ; Online: Two distinct representations of social vocalizations in the basolateral amygdala.

Gadziola, Marie A / Shanbhag, Sharad J / Wenstrup, Jeffrey J

Journal of neurophysiology

2016 Volume 115, Issue 2, Page(s) 868–886

Abstract: Acoustic communication signals carry information related to the types of social interactions by means of their "acoustic context," the sequencing and temporal emission pattern of vocalizations. Here we describe responses to natural vocal sequences in ... ...

Abstract	Acoustic communication signals carry information related to the types of social interactions by means of their "acoustic context," the sequencing and temporal emission pattern of vocalizations. Here we describe responses to natural vocal sequences in adult big brown bats (Eptesicus fuscus). We first assessed how vocal sequences modify the internal affective state of a listener (via heart rate). The heart rate of listening bats was differentially modulated by vocal sequences, showing significantly greater elevation in response to moderately aggressive sequences than appeasement or neutral sequences. Next, we characterized single-neuron responses in the basolateral amygdala (BLA) of awake, restrained bats to isolated syllables and vocal sequences. Two populations of neurons distinguished by background firing rates also differed in acoustic stimulus selectivity. Low-background neurons (<1 spike/s) were highly selective, responding on average to one tested stimulus. These may participate in a sparse code of vocal stimuli, in which each neuron responds to one or a few stimuli and the population responds to the range of vocalizations across behavioral contexts. Neurons with higher background rates (≥1 spike/s) responded broadly to tested stimuli and better represented the timing of syllables within sequences. We found that spike timing information improved the ability of these neurons to discriminate among vocal sequences and among the behavioral contexts associated with sequences compared with a rate code alone. These findings demonstrate that the BLA contains multiple robust representations of vocal stimuli that can provide the basis for emotional/physiological responses to these stimuli.
MeSH term(s)	Action Potentials ; Amygdala/cytology ; Amygdala/physiology ; Animals ; Chiroptera ; Discrimination (Psychology) ; Female ; Heart Rate ; Male ; Neurons/classification ; Neurons/physiology ; Social Behavior ; Vocalization, Animal
Language	English
Publishing date	2016-02-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00953.2015
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Article: Physiological and Behavioral Responses to Vocalization Playback in Mice.

Niemczura, Alexandra C / Grimsley, Jasmine M / Kim, Chae / Alkhawaga, Ahmad / Poth, Austin / Carvalho, Alyssa / Wenstrup, Jeffrey J

Frontiers in behavioral neuroscience

2020 Volume 14, Page(s) 155

Abstract: In mice, the caller's production of social vocalizations has been extensively studied but the effect of these vocalizations on the listener is less understood, with playback studies to date utilizing one vocalization category or listeners of one sex. ... ...

Abstract	In mice, the caller's production of social vocalizations has been extensively studied but the effect of these vocalizations on the listener is less understood, with playback studies to date utilizing one vocalization category or listeners of one sex. This study examines how several categories of mouse vocalizations affect listeners of both sexes to better understand the communicative functions of these vocal categories. We examined physiological and behavioral responses of male and female CBA/CaJ mice to playback of four social vocalization categories: ultrasonic vocalizations (USVs), low-frequency harmonic calls, mid-frequency vocalizations, and noisy calls. Based on the conditions under which these calls are emitted, we hypothesized that playback of these vocal categories would have differential effects on the listeners. In females, playback of all four vocalization categories increased stress hormone levels (corticosterone), but only the non-USV categories increased corticosterone in males. The magnitude of corticosterone increase in non-USV trials was greater in females than in males. In open field tests, all four vocal categories decreased central ambulation in males and females, indicating an increase in anxiety-related behavior. Further, we found that the proportions of USVs emitted by subjects, but not their overall calling rates, were affected by playback of some vocal categories, suggesting that vocalization categories have different communication content. These results show that, even in the absence of behavioral and acoustic contextual features, each vocal category evokes physiological and behavioral responses in mice, with some differences in responses as a function of the listener's sex and playback signal. These findings suggest that at least some of the vocal categories have distinct communicative functions.
Language	English
Publishing date	2020-09-01
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2020.00155
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Article ; Online: Neural processing of target distance by echolocating bats: functional roles of the auditory midbrain.

Wenstrup, Jeffrey J / Portfors, Christine V

Neuroscience and biobehavioral reviews

2011 Volume 35, Issue 10, Page(s) 2073–2083

Abstract: Using their biological sonar, bats estimate distance to avoid obstacles and capture moving prey. The primary distance cue is the delay between the bat's emitted echolocation pulse and the return of an echo. The mustached bat's auditory midbrain (inferior ...

Abstract	Using their biological sonar, bats estimate distance to avoid obstacles and capture moving prey. The primary distance cue is the delay between the bat's emitted echolocation pulse and the return of an echo. The mustached bat's auditory midbrain (inferior colliculus, IC) is crucial to the analysis of pulse-echo delay. IC neurons are selective for certain delays between frequency modulated (FM) elements of the pulse and echo. One role of the IC is to create these "delay-tuned", "FM-FM" response properties through a series of spectro-temporal integrative interactions. A second major role of the midbrain is to project target distance information to many parts of the brain. Pathways through auditory thalamus undergo radical reorganization to create highly ordered maps of pulse-echo delay in auditory cortex, likely contributing to perceptual features of target distance analysis. FM-FM neurons in IC also project strongly to pre-motor centers including the pretectum and the pontine nuclei. These pathways may contribute to rapid adjustments in flight, body position, and sonar vocalizations that occur as a bat closes in on a target.
MeSH term(s)	Animals ; Auditory Cortex/physiology ; Auditory Pathways/physiology ; Auditory Perception/physiology ; Brain Mapping/psychology ; Chiroptera/physiology ; Echolocation/physiology ; Inferior Colliculi/physiology ; Models, Neurological ; Neurons/physiology
Language	English
Publishing date	2011-01-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	282464-4
ISSN	1873-7528 ; 0149-7634
ISSN (online)	1873-7528
ISSN	0149-7634
DOI	10.1016/j.neubiorev.2010.12.015
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Article ; Online: Automated classification of mouse pup isolation syllables: from cluster analysis to an Excel-based "mouse pup syllable classification calculator".

Grimsley, Jasmine M S / Gadziola, Marie A / Wenstrup, Jeffrey J

Frontiers in behavioral neuroscience

2013 Volume 6, Page(s) 89

Abstract: Mouse pups vocalize at high rates when they are cold or isolated from the nest. The proportions of each syllable type produced carry information about disease state and are being used as behavioral markers for the internal state of animals. Manual ... ...

Abstract	Mouse pups vocalize at high rates when they are cold or isolated from the nest. The proportions of each syllable type produced carry information about disease state and are being used as behavioral markers for the internal state of animals. Manual classifications of these vocalizations identified 10 syllable types based on their spectro-temporal features. However, manual classification of mouse syllables is time consuming and vulnerable to experimenter bias. This study uses an automated cluster analysis to identify acoustically distinct syllable types produced by CBA/CaJ mouse pups, and then compares the results to prior manual classification methods. The cluster analysis identified two syllable types, based on their frequency bands, that have continuous frequency-time structure, and two syllable types featuring abrupt frequency transitions. Although cluster analysis computed fewer syllable types than manual classification, the clusters represented well the probability distributions of the acoustic features within syllables. These probability distributions indicate that some of the manually classified syllable types are not statistically distinct. The characteristics of the four classified clusters were used to generate a Microsoft Excel-based mouse syllable classifier that rapidly categorizes syllables, with over a 90% match, into the syllable types determined by cluster analysis.
Language	English
Publishing date	2013-01-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153 ; 1662-5153
ISSN (online)	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2012.00089
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Article ; Online: Coding the meaning of sounds: contextual modulation of auditory responses in the basolateral amygdala.

Grimsley, Jasmine M S / Hazlett, Emily G / Wenstrup, Jeffrey J

The Journal of neuroscience : the official journal of the Society for Neuroscience

2013 Volume 33, Issue 44, Page(s) 17538–17548

Abstract: Female mice emit a low-frequency harmonic (LFH) call in association with distinct behavioral contexts: mating and physical threat or pain. Here we report the results of acoustic, behavioral, and neurophysiological studies of the contextual analysis of ... ...

Abstract	Female mice emit a low-frequency harmonic (LFH) call in association with distinct behavioral contexts: mating and physical threat or pain. Here we report the results of acoustic, behavioral, and neurophysiological studies of the contextual analysis of these calls in CBA/CaJ mice. We first show that the acoustical features of the LFH call do not differ between contexts. We then show that male mice avoid the LFH call in the presence of a predator cue (cat fur) but are more attracted to the same exemplar of the call in the presence of a mating cue (female urine). The males thus use nonauditory cues to determine the meaning of the LFH call, but these cues do not generalize to noncommunication sounds, such as noise bursts. We then characterized neural correlates of contextual meaning of the LFH call in responses of basolateral amygdala (BLA) neurons from awake, freely moving mice. There were two major findings. First, BLA neurons typically displayed early excitation to all tested behaviorally aversive stimuli. Second, the nonauditory context modulates the BLA population response to the LFH call but not to the noncommunication sound. These results suggest that the meaning of communication calls is reflected in the spike discharge patterns of BLA neurons.
MeSH term(s)	Acoustic Stimulation/methods ; Action Potentials/physiology ; Amygdala/physiology ; Animals ; Auditory Perception/physiology ; Cats ; Female ; Male ; Mice ; Mice, Inbred CBA ; Vocalization, Animal/physiology
Language	English
Publishing date	2013-10-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.2205-13.2013
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Article ; Online: Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus.

Wenstrup, Jeffrey James / Nataraj, Kiran / Sanchez, Jason Tait

Frontiers in neural circuits

2012 Volume 6, Page(s) 75

Abstract: This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, ... ...

Abstract	This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, properly timed combinations of spectral elements in vocal signals and other acoustic stimuli. While these neurons are known to occur in the auditory forebrain of many vertebrate species, the work described here establishes their origin in the auditory brainstem and midbrain. Focusing on the mustached bat, we review several major findings: (1) Combination-sensitive responses involve facilitatory interactions, inhibitory interactions, or both when activated by distinct spectral elements in complex sounds. (2) Combination-sensitive responses are created in distinct stages: inhibition arises mainly in lateral lemniscal nuclei of the auditory brainstem, while facilitation arises in the inferior colliculus (IC) of the midbrain. (3) Spectral integration underlying combination-sensitive responses requires a low-frequency input tuned well below a neuron's characteristic frequency (ChF). Low-ChF neurons in the auditory brainstem project to high-ChF regions in brainstem or IC to create combination sensitivity. (4) At their sites of origin, both facilitatory and inhibitory combination-sensitive interactions depend on glycinergic inputs and are eliminated by glycine receptor blockade. Surprisingly, facilitatory interactions in IC depend almost exclusively on glycinergic inputs and are largely independent of glutamatergic and GABAergic inputs. (5) The medial nucleus of the trapezoid body (MNTB), the lateral lemniscal nuclei, and the IC play critical roles in creating combination-sensitive responses. We propose that these mechanisms, based on work in the mustached bat, apply to a broad range of mammals and other vertebrates that depend on temporally sensitive integration of information across the audible spectrum.
Language	English
Publishing date	2012-10-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452968-0
ISSN	1662-5110 ; 1662-5110
ISSN (online)	1662-5110
ISSN	1662-5110
DOI	10.3389/fncir.2012.00075
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Article ; Online: Tinnitus and underlying brain mechanisms.

Galazyuk, Alexander V / Wenstrup, Jeffrey J / Hamid, Mohamed A

Current opinion in otolaryngology & head and neck surgery

2012 Volume 20, Issue 5, Page(s) 409–415

Abstract: Purpose of review: Tinnitus is the sensation of hearing a sound when no external auditory stimulus is present. Most individuals experience tinnitus for brief, unobtrusive periods. However, chronic sensation of tinnitus affects approximately 17% (44 ... ...

Abstract	Purpose of review: Tinnitus is the sensation of hearing a sound when no external auditory stimulus is present. Most individuals experience tinnitus for brief, unobtrusive periods. However, chronic sensation of tinnitus affects approximately 17% (44 million people) of the general US population. Tinnitus, usually a benign symptom, can be constant, loud and annoying to the point that it causes significant emotional distress, poor sleep, less efficient activities of daily living, anxiety, depression and suicidal ideation/attempts. Tinnitus remains a major challenge to physicians because its pathophysiology is poorly understood and there are few management options to offer to patients. The purpose of this article is to describe the current understanding of central neural mechanisms in tinnitus and to summarize recent developments in clinical approaches to tinnitus patients. Recent findings: Recently developed animal models of tinnitus provide the possibility to determine neuronal mechanisms of tinnitus generation and to test the effects of various treatments. The latest research using animal models has identified a number of abnormal changes, in both auditory and nonauditory brain regions, that underlie tinnitus. Furthermore this research sheds light on cellular mechanisms that are responsible for development of these abnormal changes. Summary: Tinnitus remains a challenging disorder for patients, physicians, audiologists and scientists studying tinnitus-related brain changes. This article reviews recent findings of brain changes in animal models associated with tinnitus and a brief review of clinical approach to tinnitus patients.
MeSH term(s)	Animals ; Auditory Pathways/physiopathology ; Brain/physiopathology ; Female ; Forecasting ; Humans ; Male ; Needs Assessment ; Psychoacoustics ; Risk Factors ; Severity of Illness Index ; Tinnitus/etiology ; Tinnitus/physiopathology ; Tinnitus/therapy
Language	English
Publishing date	2012-08-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1232518-1
ISSN	1531-6998 ; 1068-9508
ISSN (online)	1531-6998
ISSN	1068-9508
DOI	10.1097/MOO.0b013e3283577b81
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