The Amygdala – A Hub of the Social Auditory Brain

Wenstrup, Jeffrey J.; Ghasemahmad, Zahra; Hazlett, Emily; Shanbhag, Sharad J.

doi:10.1016/b978-0-12-809324-5.24194-1

Cited by 13 publications

(10 citation statements)

References 216 publications

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“…One question is whether our effects are a result of top-down influences from regions known to be altered by ELS. For example, the amygdala has indirect effects on ACx via neuromodulatory inputs (Wenstrup et al, 2020), which may partially contribute to the reduced gap-PPI. Importantly, our neural recordings were conducted under anesthesia, minimizing the impact of top-down influences from higher-level regions (Mashour, 2014; Cai et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Mattingly

Sunthimer

et al. 2022

Preprint

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In children, early ear infections are a risk factor for later speech perception deficits. This is likely because auditory deprivation during a developmental critical period (CP) induces long-lasting deficits in perception and ACx encoding of temporally-varying sounds. CPs also create susceptibility to early-life stress (ELS) in neural regions involved with cognition and anxiety. As CP mechanisms are shared by sensory cortices and higher neural regions, ACx and temporal encoding may also be susceptible to ELS. To examine the effects of ELS on temporal processing, we developed a model of ELS in the Mongolian gerbil, a well-established model for auditory processing. ELS induction impaired the behavioral detection of short gaps in sound, which are critical for speech perception. This was accompanied by reduced neural responses to gaps in ACx, the auditory periphery, and auditory brainstem. These ELS effects presumably degrade the fidelity of sensory representations available to higher regions, and could contribute to ELS-induced problems with cognition.

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Section: Discussionmentioning

confidence: 99%

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Mattingly

Sunthimer

et al. 2022

Preprint

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“…Since both left and right amygdala are responsive to vocal stimuli in human and experimental animal studies (Wenstrup et al, 2020), we implanted microdialysis probes into the left amygdala to maintain consistency with other studies in our laboratory. Mice were anaesthetized with Isoflurane (2-4%, Abbott Laboratories, North Chicago, IL) and hair overlying the skull was removed using depilatory lotion.…”

Section: Methodsmentioning

confidence: 99%

Emotional Vocalizations Alter Behaviors and Neurochemical Release into the Amygdala

Ghasemahmad

Mrvelj

Panditi

et al. 2022

Preprint

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The basolateral amygdala (BLA), a brain center of emotional expression, contributes to acoustic communication by first interpreting the meaning of social sounds in the context of the listener s internal state, then organizing the appropriate behavioral responses. We propose that modulatory neurochemicals such as acetylcholine (ACh) and dopamine (DA) provide internal-state signals to the BLA while an animal listens to social vocalizations. We tested this in a vocal playback experiment wherein we sampled fluids within the BLA and observed behavioral responses of male and female mice while presenting highly affective vocal sequences associated with either mating or restraint behaviors. In male mice, playback of restraint vocalizations increased ACh release and decreased DA release, while playback of mating sequences evoked the opposite neurochemical release patterns. In non-estrus female mice, the ACh and DA release patterns to mating playback were similar to males. Estrous females, however, showed increased ACh, associated with vigilance, as well as increased DA, associated with reward-seeking. Across these groups, increased ACh concentration was correlated with an increase in defensive behavior. These neurochemical release patterns and several behavioral responses depended on prior experience with the mating and restraint behaviors. Our results support a model in which ACh and DA provide contextual information to sound-analyzing BLA neurons that modulates their output to downstream brain regions responsible for appropriate behavioral outcomes.

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“…The limbic system, namely, the amygdala, is affected by ELS ( Malter Cohen et al, 2013 ; Burgdorf et al, 2020 ) and plays a role in response to salient vocalizations ( Grimsley et al, 2013 ). Specifically, the basolateral amygdala (BLA) has been implicated in behavioral responses to auditory stimuli in humans, rodents, and many other animals ( Grimsley et al, 2013 ; Wenstrup et al, 2020 ). Another region that shapes auditory perception and is known to be affected by ELS is the PFC, which plays a vital role in attention, decision-making, and learning ( Krugers et al, 2017 ; Kolk and Rakic, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Early-life stress affects Mongolian gerbil interactions with conspecific vocalizations in a sex-specific manner

Hardy

Hart

Rosen

2023

Front. Behav. Neurosci.

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During development, early-life stress (ELS) impairs cognition, learning, and emotional regulation, in part by disrupting neural circuitry in regions underlying these higher-order functions. In addition, our recent work indicates that ELS also alters simple sensory perception: ELS impaired auditory perception and neural encoding of short gaps in sounds, which are essential for vocal communication. The combination of higher-order and basic sensory disruption suggests that ELS is likely to affect both the perception and interpretation of communication signals. We tested this hypothesis by measuring behavioral responses to conspecific vocalizations (those emitted by other gerbils) in ELS and untreated Mongolian gerbils. Because stress effects often differ by sex, we separately examined females and males. To induce ELS, pups were intermittently maternally separated and restrained from post-natal days (P) 9–24, a time window when the auditory cortex is most sensitive to external disruption. We measured the approach responses of juvenile (P31–32) gerbils to two types of conspecific vocalizations: an alarm call, which is emitted to alert other gerbils of a potential threat, and the prosocial contact call, which is emitted near familiar gerbils, especially after separation. Control males, Control females, and ELS females approached a speaker emitting pre-recorded alarm calls, while ELS males avoided this source, suggesting that ELS affects the response to alarm calls in male gerbils. During playback of the pre-recorded contact call, Control females and ELS males avoided the sound source, while Control males neither approached nor avoided, and ELS females approached the sound. These differences cannot be accounted for by changes in locomotion or baseline arousal. However, ELS gerbils slept more during playback, suggesting that ELS may reduce arousal during vocalization playback. Further, male gerbils made more errors than females on a measure of working memory, but the sex difference of cognition in this context may stem from novelty aversion rather than impaired memory. These data indicate that ELS influences behavioral responses to ethologically relevant communication sounds in a sex-specific manner, and are among the first to demonstrate an altered response to auditory stimuli following ELS. Such changes may arise from differences in auditory perception, cognition, or a combination of factors, and suggest that ELS may affect auditory communication in human adolescents.

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The Amygdala – A Hub of the Social Auditory Brain

Cited by 13 publications

References 216 publications

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Emotional Vocalizations Alter Behaviors and Neurochemical Release into the Amygdala

Early-life stress affects Mongolian gerbil interactions with conspecific vocalizations in a sex-specific manner

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