Unconditioned stimulus pathways to the amygdala: Effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala

Lanuza, Enrique; Moncho-Bogani, José; LeDoux, Joseph E.

doi:10.1016/j.neuroscience.2008.06.028

Cited by 71 publications

(43 citation statements)

References 56 publications

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“…These pathways play a central role in rodent behavior [e.g. (Romanski and LeDoux, 1992; Lanuza et al, 2004; Lanuza et al, 2008)]. In primates, pathways that involve high-order thalamic nuclei, association cortices, and amygdala provide another route for the perception and evaluation of complex salient stimuli (Morris et al, 1998; Compton, 2003; Williams et al, 2006; Jones, 2007; Straube et al, 2007; Pessoa, 2008; Pessoa and Adolphs, 2010).…”

Section: Discussionmentioning

confidence: 99%

Pathways for Emotions and Attention Converge on the Thalamic Reticular Nucleus in Primates

Zikopoulos¹,

Barbas²

2012

J. Neurosci.

166

137

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How do emotional events readily capture our attention? To address this question we used neural tracers to label pathways linking areas involved in emotional and attentional processes in the primate brain (Macaca mulatta). We report that a novel pathway from the amygdala, the brain's emotional center, targets the inhibitory thalamic reticular nucleus (TRN), a key node in the brain's attentional network. The amygdalar pathway formed unusual synapses close to cell bodies of TRN neurons, and had more large and efficient terminals than pathways from the orbitofrontal cortex and the thalamic mediodorsal nucleus, which similarly innervated extensive TRN sites. The robust amygdalar pathway provides a mechanism for rapid shifting of attention to emotional stimuli. Acting synergistically, pathways from the amygdala and orbitofrontal cortex provide a circuit for purposeful assessment of emotional stimuli. The different pathways to TRN suggest distinct mechanisms of attention to external and internal stimuli that may be differentially disrupted in anxiety and mood disorders and may be selectively targeted for therapeutic interventions.

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Section: Discussionmentioning

confidence: 99%

Pathways for Emotions and Attention Converge on the Thalamic Reticular Nucleus in Primates

Zikopoulos¹,

Barbas²

2012

J. Neurosci.

166

137

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“…In our current fear-conditioning experiments, we find learning-specific FTL expression in the same region of the LAvl as previously reported (Wilson and Murphy 2009). Other studies have reported c-fos or other immediate early gene expression in LA following fear conditioning or footshock Rosen et al 1998;Savonenko et al 1999;Schettino and Otto 2001;Radwanska et al 2002;Majak and Pitkanen 2003;Holahan and White 2004;Knapska et al 2007;Lanuza et al 2008;Furlong et al 2010). However, these studies also suggested that this expression was either not specifically fear-learning related, or the cause of this expression could not be determined.…”

Section: Learning-specific Neurons In the Lavlmentioning

confidence: 94%

Context fear learning specifically activates distinct populations of neurons in amygdala and hypothalamus

Trogrlic¹,

Wilson²,

Newman³

et al. 2011

Learn. Mem.

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The identity and distribution of neurons that are involved in any learning or memory event is not known. In previous studies, we identified a discrete population of neurons in the lateral amygdala that show learning-specific activation of a c-fos-regulated transgene following context fear conditioning. Here, we have extended these studies to look throughout the amygdala for learning-specific activation. We identified two further neuronal populations, in the amygdalo-striatal transition area and medial amygdala, that show learning-specific activation. We also identified a population of hypothalamic neurons that show strong learning-specific activation. In addition, we asked whether these neurons are activated following recall of fear-conditioning memory. None of the populations of neurons we identified showed significant memory-recallrelated activation. These findings suggest that a series of discrete populations of neurons are involved in fear learning in amygdala and hypothalamus. The lack of reactivation during memory recall suggests that these neurons either do not undergo substantial change following recall, or that c-fos is not involved in any such activation and change.Pavlovian fear conditioning is one of the best-characterized models for the study of learning and memory and its neural correlates. It involves the association of a neutral stimulus, the conditioned stimulus (CS) such as a sound or context, with an aversive unconditioned stimulus (US) such as a footshock. Fear conditioning is quite robust, and a large percentage of trained animals show fear learning. It can be examined with respect to several excellent nonlearning controls. Some of the major areas of the brain that are necessary for expression of fear conditioning have been determined by lesioning experiments, with the amygdala playing a central role in the process (Pitkanen et al. 1997;LeDoux 2000;Sah et al. 2003;Fanselow and Poulos 2005;Ehrlich et al. 2009).A large body of evidence implicates the lateral amygdala in the formation and storage of fear memories in the amygdala (LeDoux 1993;Fanselow and LeDoux 1999;Maren and Quirk 2004;Pare et al. 2004;Rodrigues et al. 2004); however, this region does not act in isolation. Anterograde and retrograde tracing studies have yielded a plethora of amygdalar efferents and afferents. The amygdala itself is comprised of several heavily interconnected nuclei and receives a massive array of both cortical (McDonald 1998) and subcortical inputs (Pitkanen et al. 1997;Sah et al. 2003). The amygdala also receives modulatory monoaminergic input from hypothalamic nuclei (Asan et al. 2005); however, this remains poorly characterized.In moving beyond basic functional neuroanatomy, progress in our understanding of the brain requires not only a comprehension of the mechanisms of plasticity, but also of the localized circuitry involved in specific behaviors. Our previous development of the transgenic fos-tau-lacZ (FTL) mouse (Wilson et al. 2002;Murphy et al. 2007) has emerged as an excellent tool for visualizing fun...

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“…Some studies suggest that the sensory discriminative component of the nociceptive information is conveyed to the BLA via a spino-thalamic tract composed of lamina I spinal cord neurons targeting the posterior intralaminar thalamic nucleus (PIN), which in turn sends excitatory projections to the BLA (Asede et al 2015;Bienvenu et al 2015). However, this hypothesis has been challenged by studies showing that fiber-sparing lesions in this area do not impair footshock learning (Brunzell and Kim 2001;Lanuza et al 2008;Herry and Johansen 2014). An alternative input carrying nociceptive information to the BLA might originate from the PAG through midline thalamic or other cortical relays, because the PAG integrates nociceptive inputs from the spinal and trigeminal dorsal horn (Johansen et al 2010) and PAG electrical stimulation is sufficient to instruct BLA-dependent fear learning (Di Scala et al 1987;Kim et al 2013).…”

Section: Noxious Stimulimentioning

confidence: 99%

The neural circuits of innate fear: detection, integration, action, and memorization

2016

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How fear is represented in the brain has generated a lot of research attention, not only because fear increases the chances for survival when appropriately expressed but also because it can lead to anxiety and stress-related disorders when inadequately processed. In this review, we summarize recent progress in the understanding of the neural circuits processing innate fear in rodents. We propose that these circuits are contained within three main functional units in the brain: a detection unit, responsible for gathering sensory information signaling the presence of a threat; an integration unit, responsible for incorporating the various sensory information and recruiting downstream effectors; and an output unit, in charge of initiating appropriate bodily and behavioral responses to the threatful stimulus. In parallel, the experience of innate fear also instructs a learning process leading to the memorization of the fearful event. Interestingly, while the detection, integration, and output units processing acute fear responses to different threats tend to be harbored in distinct brain circuits, memory encoding of these threats seems to rely on a shared learning system.

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Unconditioned stimulus pathways to the amygdala: Effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala

Cited by 71 publications

References 56 publications

Pathways for Emotions and Attention Converge on the Thalamic Reticular Nucleus in Primates

Pathways for Emotions and Attention Converge on the Thalamic Reticular Nucleus in Primates

Context fear learning specifically activates distinct populations of neurons in amygdala and hypothalamus

The neural circuits of innate fear: detection, integration, action, and memorization

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