Coding the Meaning of Sounds: Contextual Modulation of Auditory Responses in the Basolateral Amygdala

Grimsley, Jasmine M. S.; Hazlett, Emily; Wenstrup, Jeffrey J.

doi:10.1523/jneurosci.2205-13.2013

Cited by 55 publications

(77 citation statements)

References 45 publications

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“…Romanski and Averbeck suggested that one way to demonstrate semantic categorization in the brain would be to show that sounds with similar acoustic morphology but different semantic context evoke different neural responses (Romanski & Averbeck, 2009). Interestingly, the activity of neurons in the male mouse basolateral amygdala in response to the same female vocalization is modulated by the context (predator cue vs. mating cue), whereas it is not when the sound presented in these two contexts is a burst of noise (Grimsley et al, 2013). This differential neuronal activity is correlated with male mouse behavior in response to the same vocalization (escape in the presence of the predator cue, and approach in the presence of the mating cue).…”

Section: Disentangling Semantic Categorization From Acoustic Categorimentioning

confidence: 99%

Meaning in the avian auditory cortex: neural representation of communication calls

Elie

Theunissen

2015

Eur J of Neuroscience

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Understanding how the brain extracts the behavioral meaning carried by specific vocalization types that can be emitted by various vocalizers and in different conditions is a central question in auditory research. This semantic categorization is a fundamental process required for acoustic communication and presupposes discriminative and invariance properties of the auditory system for conspecific vocalizations. Songbirds have been used extensively to study vocal learning, but the communicative function of all their vocalizations and their neural representation has yet to be examined. In our research, we first generated a library containing almost the entire zebra finch vocal repertoire and organized communication calls along 9 different categories based on their behavioral meaning. We then investigated the neural representations of these semantic categories in the primary and secondary auditory areas of 6 anesthetized zebra finches. To analyze how single units encode these call categories, we described neural responses in terms of their discrimination, selectivity and invariance properties. Quantitative measures for these neural properties were obtained using an optimal decoder based both on spike counts and spike patterns. Information theoretic metrics show that almost half of the single units encode semantic information. Neurons achieve higher discrimination of these semantic categories by being more selective and more invariant. These results demonstrate that computations necessary for semantic categorization of meaningful vocalizations are already present in the auditory cortex and emphasize the value of a neuro-ethological approach to understand vocal communication.

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Section: Disentangling Semantic Categorization From Acoustic Categorimentioning

confidence: 99%

Meaning in the avian auditory cortex: neural representation of communication calls

Elie

Theunissen

2015

Eur J of Neuroscience

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“…Studies on mice have shown that neurons in the basolateral amygdala exhibit early excitation to sociallyrelevant auditory stimuli (conspecific calls), and that this response is modulated by the non-auditory context (e.g. threatening or mating cues) (Grimsley et al, 2013). Importantly, the non-auditory context does not modulate the amygdalar response to non-socially-relevant sounds (e.g.…”

Section: Amygdalamentioning

confidence: 99%

Subcortical processing in auditory communication

2015

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a b s t r a c tThe voice is a rich source of information, which the human brain has evolved to decode and interpret. Empirical observations have shown that the human auditory system is especially sensitive to the human voice, and that activity within the voice-sensitive regions of the primary and secondary auditory cortex is modulated by the emotional quality of the vocal signal, and may therefore subserve, with frontal regions, the cognitive ability to correctly identify the speaker's affective state. So far, the network involved in the processing of vocal affect has been mainly characterised at the cortical level. However, anatomical and functional evidence suggests that acoustic information relevant to the affective quality of the auditory signal might be processed prior to the auditory cortex.Here we review the animal and human literature on the main subcortical structures along the auditory pathway, and propose a model whereby the distinction between different types of vocal affect in auditory communication begins at very early stages of auditory processing, and relies on the analysis of individual acoustic features of the sound signal. We further suggest that this early feature-based decoding occurs at a subcortical level along the ascending auditory pathway, and provides a preliminary coarse (but fast) characterisation of the affective quality of the auditory signal before the more refined (but slower) cortical processing is completed.

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“…The ratio of stimulus-selective cells to all recorded cells was larger in the surrounding arcopallium (34.1%) than in the TnA (20.3%), suggesting that neurons in this area can represent behavioral relevance of stimuli and be involved in recognizing vocalizations and controlling successive behaviors. Recently, neural activity in the amygdala, especially in the lateral or basolateral subdivision, has been investigated in rodents and bats [Naumann and Kanwal, 2011;Gadziola et al, 2012Gadziola et al, , 2016Parsana et al, 2012;Peterson and Wenstrup, 2012;Grimsley et al, 2013]. In the rat lateral amygdala, it has been known that neurons respond to the cue tones in the fear conditioning [LeDoux et al, 1990].…”

Section: Evolutional Perspectivementioning

confidence: 99%

“…The authors reported that 82% of recorded cells were auditory responsive, which is comparable to our results in the TnA (68.7%) and in the surrounding arcopallium (72.4%). Grimsley et al [2013] demonstrated that neurons in the mouse basolateral amygdala are activated when listening to behaviorally aversive vocalizations and that the activity is modulated by visual cues associated with predation. In bats, the neurons in the lateral [Gadziola et al, 2012] or basolateral amygdala [Naumann and Kanwal, 2011;Peterson and Wenstrup, 2012;Gadziola et al, 2016] respond selectively to specific social calls.…”

Section: Evolutional Perspectivementioning

confidence: 99%

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium

Fujii

Ikebuchi²,

Okanoya³

2016

Brain Behav Evol

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Many species of animals communicate with others through vocalizations. Over time, these species have evolved mechanisms to respond to biologically relevant vocal sounds via adaptive behaviors. Songbirds provide a good opportunity to search for the neural basis of this adaptation, because they interact with others through a variety of vocalizations in complex social relationships. The nucleus taeniae of the amygdala (TnA) is a structure located in the ventromedial arcopallium, which is akin to the mammalian medial amygdala. Studies on the anatomy and function of this nucleus have led to the speculation that the TnA is one of the possible neural substrates that represents the relevance of acoustic stimuli related to behavior. However, neural responses in this nucleus to auditory stimuli have not been studied in depth. To give a detailed description about auditory responses of the TnA in the songbird, we conducted neural recordings from the TnA and the adjacent arcopallium in adult male and female Bengalese finches under anesthesia. The birds were exposed to auditory stimuli including natural vocalizations as well as synthesized noise. We demonstrated that a substantial population of neurons in the TnA and the adjacent arcopallium responded to vocal sounds and that some neurons were selectively activated to specific stimuli. Proportions of responsive cells and stimulus-selective cells were larger in males than in females. In addition, a larger ratio of selective cells was observed in the arcopallium compared to the TnA. These findings support the idea that neuronal activity in the TnA and the neighboring area represents behavioral relevance of sounds. Further studies in electrophysiology combined with evidence from other fields, such as region-specific gene expression patterns, are required to fully understand the functions of the TnA as well as the evolution of the amygdala in songbirds and vertebrate animals.

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Coding the Meaning of Sounds: Contextual Modulation of Auditory Responses in the Basolateral Amygdala

Cited by 55 publications

References 45 publications

Meaning in the avian auditory cortex: neural representation of communication calls

Meaning in the avian auditory cortex: neural representation of communication calls

Subcortical processing in auditory communication

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium

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