Activation of phenotypically-distinct neuronal subpopulations of the rat amygdala following exposure to predator odor

Butler, Ryan K.; Sharko, Amanda C.; Oliver, Elisabeth M.; Brito-Vargas, Paul; Kaigler, Kris F.; Fadel, Jim R.; Wilson, Marlene A.

doi:10.1016/j.neuroscience.2010.12.001

Cited by 52 publications

(77 citation statements)

References 55 publications

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“…These cell subpopulations are mainly nonpyramidal GABAergic interneurons (McDonald and Mascagni, 2001) and are involved in fear and anxiety processes (Butler et al, 2011;Wolff et al, 2014). In agreement with previous studies, approximately 80% of PV neurons exhibited colocalization with CB, and the number of neurons expressing PV and/or CB was not modified in mice treated with the OX1R antagonist (Figure 2A).…”

Section: Ox1r Blockade Enhances the Activation Of Local Interneurons supporting

confidence: 92%

“…Nonpyramidal GABAergic interneurons within the BLA can be divided considering the content of several calcium-binding proteins such as CB and/or PV (McDonald and Mascagni, 2001). These cell subtypes have been previously involved in the regulation of fear behaviors (Butler et al, 2011;Wolff et al, 2014) and could differentially modulate neuronal circuits related to fear conditioning and extinction processes. The administration of SB334867 increased the activation of neurons containing CB, but not PV, during the extinction of fear.…”

Section: Discussionmentioning

confidence: 99%

“…These cell populations, functionally defined as "fear neurons" and "extinction neurons," overlap with 2 different anatomically defined subtypes of BLA neurons projecting to prelimbic medial prefrontal cortex (PL) or IL, respectively (Senn et al, 2014). Nonpyramidal GABAergic interneurons within the BLA can be classified by the content of several calcium-binding proteins such as calbindin (CB) and/or parvalbumin (PV) (McDonald and Mascagni, 2001;Capogna, 2014), which could differentially control these neuronal circuits since they are involved in fear and anxiety (Butler et al, 2011;Wolff et al, 2014). Whether orexins affect these circuits and GABAergic interneuron subpopulations during emotional memory processes remain unexplored.…”

Section: Introductionmentioning

confidence: 99%

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Facilitation of contextual fear extinction by orexin-1 receptor antagonism is associated with the activation of specific amygdala cell subpopulations

Flores¹,

Herry²,

Maldonado³

et al. 2017

European Neuropsychopharmacology

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Background: Orexins are hypothalamic neuropeptides recently involved in the regulation of emotional memory. The basolateral amygdala, an area orchestrating fear memory processes, appears to be modulated by orexin transmission during fear extinction. However, the neuronal types within the basolateral amygdala involved in this modulation remain to be elucidated. Methods: We used retrograde tracing combined with immunofluorescence techniques in mice to identify basolateral amygdala projection neurons and cell subpopulations in this brain region influenced by orexin transmission during contextual fear extinction consolidation. Results: Treatment with the orexin-1 receptor antagonist SB334867 increased the activity of basolateral amygdala neurons projecting to infralimbic medial prefrontal cortex during fear extinction. GABAergic interneurons expressing calbindin, but not parvalbumin, were also activated by orexin-1 receptor antagonism in the basolateral amygdala. Conclusions: These data identify neuronal circuits and cell populations of the amygdala associated with the facilitation of fear extinction consolidation induced by the orexin-1 receptor antagonist SB334867.

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Section: Ox1r Blockade Enhances the Activation Of Local Interneurons supporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Facilitation of contextual fear extinction by orexin-1 receptor antagonism is associated with the activation of specific amygdala cell subpopulations

Flores¹,

Herry²,

Maldonado³

et al. 2017

European Neuropsychopharmacology

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“…The central amygdala (CeA) has largely been thought of as noncritical for the expression of predator odor-induced fear behavior (Hunt et al 2009;Li et al 2004;McGregor et al 2004). However, fox urine exposure alters monoamine activity in the CeA (Hayley et al 2001), and ferret odor has been documented to result in the activation of a phenotypically distinct neuronal population in the CeA (Butler et al 2011). Evidence for the role of the medial amygdala (MeA) in predator odor processing is more consistent, with lesion (Blanchard et al 2005;Li et al 2004;Takahashi et al 2007) and neural activation Hunt et al 2009;McGregor et al 2004) studies indicating a pivotal role in the generation and regulation of predator odor-induced fear behavior, particularly within the posteroventral part of the MeA.…”

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confidence: 99%

In vivo electrophysiological recordings in amygdala subnuclei reveal selective and distinct responses to a behaviorally identified predator odor

Govic

Paolini

2015

Journal of Neurophysiology

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Govic A, Paolini AG. In vivo electrophysiological recordings in amygdala subnuclei reveal selective and distinct responses to a behaviorally identified predator odor. J Neurophysiol 113: 1423-1436, 2015. First published December 4, 2014 doi:10.1152/jn.00373.2014.-Chemosensory cues signaling predators reliably stimulate innate defensive responses in rodents. Despite the well-documented role of the amygdala in predator odor-induced fear, evidence for the relative contribution of the specific nuclei that comprise this structurally heterogeneous structure is conflicting. In an effort to clarify this we examined neural activity, via electrophysiological recordings, in amygdala subnuclei to controlled and repeated presentations of a predator odor: cat urine. Defensive behaviors, characterized by avoidance, decreased exploration, and increased risk assessment, were observed in adult male hooded Wistar rats (n ϭ 11) exposed to a cloth impregnated with cat urine. Electrophysiological recordings of the amygdala (777 multiunit clusters) were subsequently obtained in freely breathing anesthetized rats exposed to cat urine, distilled water, and eugenol via an air-dilution olfactometer. Recorded units selectively responded to cat urine, and frequencies of responses were distributed differently across amygdala nuclei; medial amygdala (MeA) demonstrated the greatest frequency of responses to cat urine (51.7%), followed by the basolateral and basomedial nuclei (18.8%) and finally the central amygdala (3.0%). Temporally, information transduction occurred primarily from the cortical amygdala and MeA (ventral divisions) to other amygdala nuclei. Interestingly, MeA subnuclei exhibited distinct firing patterns to predator urine, potentially revealing aspects of the underlying neurocircuitry of predator odor processing and defensiveness. These findings highlight the critical involvement of the MeA in processing olfactory cues signaling predator threat and converge with previous studies to indicate that amygdala regulation of predator odor-induced fear is restricted to a particular set of subnuclei that primarily include the MeA, particularly the ventral divisions.

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“…In order to assess the influence of areas previously identified as important in the modulation of scenery perception, four brain areas were chosen in the following volumes of interest (VOIs): the anterior cingulate cortex (ACC) (x = ±9, y = 41, z = 8), vmPFC (x = −1, y = 51, z = −1), amygdala (x = ±23, y = 0, z = −15) and PAG (x = −6, y = −30, z = −5). The choice was based on previous nonhuman [26,27] and human studies [13,14] and, when needed, MNI coordinates were transformed into the Talairach space using Brett algorithm [28]. A box was drawn around each of these coordinates, whose size varied from 125 to 719, depending on the anatomical location and the specificity required.…”

Section: Discussionmentioning

confidence: 99%

Behavioral and neuroimaging responses induced by mental imagery of threatening scenarios

Shuhama

Rondinoni

Araújo

et al. 2016

Behavioural Brain Research

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h i g h l i g h t s• Imaginary of imminent threat scenarios increased fMRI signal of the dorsal midbrain.• Activity in vmPFC was reduced during the imagination of imminent threat scenarios.• Activation pattern was consistent with animal data and actual threat situations.• Imminent and potential threats modulate brain structures related to fear and anxiety.• Mental imagery is a reliable method to study the neurobiology of behavioral processes. Functional neuroimaging studies have shown that actual situations of uncertain or distant threats increase the activity of forebrain regions, whereas proximal threats increase the activity of the dorsal midbrain. This experiment aimed at testing the hypothesis that brain activity elicited by imagined scenarios of threats with two different magnitudes, potential and imminent, resembles that found in response to actual threats. First, we measured subjective responses to imagined scenarios of potential and imminent threats compared with neutral and pleasant scenarios. The same scenarios were used as a paradigm in a functional magnetic resonance imaging experiment. Behavioral results show that the scenarios draw a gradient of hedonic valence and arousal dimensions. Both potential and imminent threat scenarios increased subjective anxiety; the imminent threat scenario also increased feelings of discomfort and bodily symptoms. The functional magnetic resonance imaging results revealed modulations of BOLD signal in the ventromedial prefrontal cortex by potential threat and in the periaqueductal gray matter by imminent threat. These results agree with previously reported evidence using actual threat situations, indicating that mental imagery is a reliable method for studying the functional neuroanatomy of relevant behavioral processes.

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Activation of phenotypically-distinct neuronal subpopulations of the rat amygdala following exposure to predator odor

Cited by 52 publications

References 55 publications

Facilitation of contextual fear extinction by orexin-1 receptor antagonism is associated with the activation of specific amygdala cell subpopulations

Facilitation of contextual fear extinction by orexin-1 receptor antagonism is associated with the activation of specific amygdala cell subpopulations

In vivo electrophysiological recordings in amygdala subnuclei reveal selective and distinct responses to a behaviorally identified predator odor

Behavioral and neuroimaging responses induced by mental imagery of threatening scenarios

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