Amygdala Central Nucleus Function Is Necessary for Learning, but Not Expression, of Conditioned Auditory Orienting.

Groshek, Frank; Kerfoot, Erin C.; McKenna, Vanessa; Polackwich, A. Scott; Gallagher, Michela; Holland, Peter C.

doi:10.1037/0735-7044.119.1.202

Cited by 31 publications

(39 citation statements)

References 54 publications

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“…Based on previous findings in our laboratory (24), we expected the dorsal amygdala and anterior hippocampus to be activated both in anticipation of and response to aversive pictures, consistent with the idea that there is one system that governs both processes (26,43). Work highlighting the role of the amygdala, especially the dorsally located central nucleus of the amygdala (CeA), in modulating attention and perception of motivationally salient events (2,3,7,(44)(45)(46)(47)(48)(49)(50)(51)(52) leads to the prediction that dorsal amygdala activation in anticipation of and response to aversive pictures may show a particularly strong association with encoding and immediate recognition of those pictures. Research establishing the hippocampus as a primary neural substrate for episodic memory (53)(54)(55)(56)(57) suggests that anterior hippocampus activation in this study would predict both immediate and delayed recognition.…”

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confidence: 76%

The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory

Mackiewicz

Sarinopoulos

Cleven

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

138

140

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Prior research has shown memory is enhanced for emotional events. Key brain areas involved in emotional memory are the amygdala and hippocampus, which are also recruited during aversion and its anticipation. This study investigated whether anticipatory processes signaling an upcoming aversive event contribute to emotional memory. In an event-related functional MRI paradigm, 40 healthy participants viewed aversive and neutral pictures preceded by predictive warning cues. Participants completed a surprise recognition task directly after functional MRI scanning or 2 weeks later. In anticipation of aversive pictures, bilateral dorsal amygdala and anterior hippocampus activations were associated with better immediate recognition memory. Similar associations with memory were observed for activation of those areas in response to aversive pictures. Anticipatory activation predicted immediate memory over and above these associations for picture viewing. Bilateral ventral amygdala activations in response to aversive pictures predicted delayed memory only. We found that previously reported sex differences of memory associations with left amygdala for women and with right amygdala for men were confined to the ventral amygdala during picture viewing and delayed memory. Results support an established animal model elucidating the functional neuroanatomy of the amygdala and hippocampus in emotional memory, highlight the importance of anticipatory processes in such memory for aversive events, and extend neuroanatomical evidence of sex differences for emotional memory.aversion ͉ expectancy ͉ functional MRI ͉ neuroimaging ͉ recognition memory M emories for emotional events are more persistent and vivid than other memories (1-3). Previous research has shown that the amygdala and hippocampus are necessary for the enhanced memory observed for emotional material and contexts (4-12). Recent neuroimaging studies have shown that amygdala and hippocampus activation during encoding of emotional stimuli is related to better recollection of those stimuli (13-23). Other studies have shown that these areas already are recruited in anticipation of aversive emotional stimuli (24-29). Moreover, emotional arousal and emotional influences on attention and perception, which are emphasized in the literature on emotional memory (2-7, 30, 31), are key features of anticipating aversion. Specifically, the anticipation of aversive events is associated with heightened arousal, as indexed by startle (25,(32)(33)(34)(35) and the modulation of perception and attention (36-39) that, in turn, is important for memory encoding (40-42).The present functional MRI (fMRI) study tested whether activation of the amygdala and hippocampus during the anticipation of aversive events is related to subsequent memory of these events. Based on previous findings in our laboratory (24), we expected the dorsal amygdala and anterior hippocampus to be activated both in anticipation of and response to aversive pictures, consistent with the idea that there is one system that governs ...

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mentioning

confidence: 76%

The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory

Mackiewicz

Sarinopoulos

Cleven

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

138

140

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“…In the same study, the authors showed that the medial CeA cells retrogradely labeled from the SNc expressed an immediate-early gene, FOS, after conditioned orienting responses, demonstrating the direct involvement of the CeA to SNc projection in conditioned orienting. Furthermore, a series of studies demonstrated time dependencies such as those observed by Holland and Gallagher (2006): CeA function was critical only at the time of acquisition (McDannald et al, 2004;Groshek et al, 2005), and function of another brain region, the dorsal lateral striatum, was critical only at the time of expression of that learned response (Han et al, 1997). Most important, SNc function was critical to both the acquisition and expression of that behavior (El Almamy and Holland, 2006).…”

Section: Discussionmentioning

confidence: 99%

Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

Lee¹,

Youn²,

O³

et al. 2006

J. Neurosci.

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Coding of prediction error by midbrain dopamine neurons has been examined extensively in the framework of associative learning theory. Most of this research has focused on the role of prediction error in determining the reinforcement value of unconditioned stimuli: poorly predicted ("surprising") outcomes are more effective reinforcers and produce a greater dopamine response than well predicted outcomes. However, surprise also enhances attention to cues that signal poorly predicted outcomes. Previous reports from our laboratories demonstrated that circuitry, including the amygdala central nucleus (CeA), the cholinergic neurons of the substantia innominata/ nucleus basalis region, and their innervation of the posterior parietal cortex, is critical to these surprise-induced enhancements of attention in associative learning. The present study considered the origin of prediction error information important for the operation of this system by examining the effects of disrupting communication between the midbrain substantia nigra pars compacta (SNc) and the CeA. Rats received unilateral lesions of the SNc and lesions of the CeA in either the contralateral or ipsilateral hemisphere. Contralateral lesions eliminated the surprise-induced enhancement of attention and learning that was displayed by rats with ipsilateral control lesions. These results show that SNc-CeA communication is critical to mechanisms by which the coding of prediction error by midbrain dopamine neurons is translated into enhancement of attention and learning modulated by the cholinergic system.

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“…However, it has been shown that, unlike instrumental responses on discrimination tasks, the expression of conditioned cardiovascular responses in Pavlovian tasks depends on an intact amygdala (33). Moreover, the acquisition of various conditioned behaviors including CSelicited approach (34) and orienting responses also depend on an intact amygdala (35,36), despite their expression being amygdala-independent (M.S.M., K.B., Y. Mikheenko, and A.C.R., unpublished results and refs. [35][36][37].…”

Section: Discussionmentioning

confidence: 99%

Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex

Reekie

Braesicke

Man

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Successful adaptation to changes in an animal's emotional and motivational environment depends on behavioral flexibility accompanied by changes in bodily responses, e.g., autonomic and endocrine, which support the change in behavior. Here, we identify the orbitofrontal cortex (OFC) as pivotal in the flexible regulation and coordination of behavioral and autonomic responses during adaptation. Using an appetitive Pavlovian task, we demonstrate that OFC lesions in the marmoset (i) impair an animal's ability to rapidly suppress its appetitive cardiovascular arousal upon termination of a conditioned stimulus and (ii) cause an uncoupling of the behavioral and autonomic components of the adaptive response after reversal of the reward contingencies. These findings highlight the role of the OFC in emotional regulation and are highly relevant to our understanding of disorders such as schizophrenia and autism in which uncoupling of emotional responses may contribute to the experiential distress and disadvantageous behavior associated with these disorders.behavioral inhibition ͉ emotion ͉ reversal learning T he orbitofrontal cortex (OFC) has long been implicated in behavioral f lexibility as measured by tests of discrimination reversal learning and extinction (1, 2). In reversal learning, an animal is first taught to respond to one of two visual stimuli to receive food reward, a response to the other being unrewarded. Lesions of the OFC do not affect initial acquisition of the visual discrimination, but the ability to alter responding when the association between the stimuli and reward is reversed is markedly impaired across a range of species (3-9). Similarly, animals with OFC lesions display prolonged responding during extinction when the response no longer results in the receipt of food reward (1, 10, 11). However, an alteration in behavioral output is just one component of the overall adaptive response of an animal to changes in its environment. It is important to recognize that behavioral adaptation is accompanied by alterations in the bodily state, including autonomic and endocrine activity, appropriate to the motivational and emotional context. Thus, Pavlov showed that dogs stopped salivating to a buzzer when it no longer predicted reward (12), and, had the behavioral response also been measured, it would have presumably shown that they stopped approaching the buzzer too. Indeed, if, despite inhibiting their salivation during extinction, Pavlov's dogs found themselves still approaching the buzzer, or vice versa, such incongruency between the somatic and autonomic feedback might be expected to produce emotional ambiguity, an issue that will be considered in more detail in Discussion.Currently, we have very little understanding of the neural circuitry underlying the coordination of behavioral and bodily responses in adaptive responding. Although the OFC is critical for behavioral adaptation, its role in the overall coordination of the adaptive response is unknown. Indeed, few studies have investigated the role of the O...

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Amygdala Central Nucleus Function Is Necessary for Learning, but Not Expression, of Conditioned Auditory Orienting.

Cited by 31 publications

References 54 publications

The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory

The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory

Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex

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