Involvement of the amygdala in classical conditioning of eyeblink response in the rat

Neufeld, Michal; Mintz, Matti

doi:10.1016/s0006-8993(00)03123-1

Cited by 58 publications

(52 citation statements)

References 12 publications

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“…Acute stress facilitates acquisition of many associative learning tasks, such as fear conditioning (Maier, 1990;Cordero et al, 2003;Rodríguez Manzanares et al, 2005) and eyeblink conditioning (Shors et al, 1992;Beylin and Shors, 1998;Neufeld and Mintz, 2001;Shors, 2001). Based on its established role in emotions and emotional learning, the basolateral nucleus of the amygdala (BLA) is a structure likely to modulate learning after stress.…”

Section: Introductionmentioning

confidence: 99%

“…Based on its established role in emotions and emotional learning, the basolateral nucleus of the amygdala (BLA) is a structure likely to modulate learning after stress. The BLA is critically involved in the stress-induced modulation of classical conditioning (Neufeld and Mintz, 2001; Rodríguez Manzanares et al, 2005). Antagonism of NMDA receptors within the BLA at the time of stress exposure blocked the facilitation of eyeblink conditioning .…”

Section: Introductionmentioning

confidence: 99%

“…In tasks such as passive avoidance, the BLA positively modulates memory consolidation Roozendaal et al, 2002) and also modulates activity in the hippocampus during learning and stress (Vazdarjanova and McGaugh, 1999;Kim et al, 2001;Huff and Rudy, 2004;Blankenship et al, 2005;Korz and Frey, 2005). In general, an intact amygdala is necessary for stress-induced facilitation of classical fear and eyeblink conditioning Neufeld and Mintz, 2001;Rodríguez Manzanares et al, 2005). It is important to note that these reports were conducted exclusively in male animals Neufeld and Mintz, 2001;Rodríguez Manzanares et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females

Waddell

Bangasser²,

Shors

2008

J. Neurosci.

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The basolateral nucleus of the amygdala (BLA) has been implicated in the modulation of learning after stress. Acute inescapable stress enhances classical eyeblink conditioning in male rats, whereas the same stressor impairs eyeblink conditioning in female rats. The experiments here directly assessed whether inactivation of the BLA during stress exposure would block both the stress-induced facilitation in males and the retardation of eyeblink conditioning in females. To this end, the BLA was temporarily inactivated by infusion of the GABA agonist muscimol before acute stressor exposure. All rats were trained in a different context 24 h later. Males infused with muscimol before the stressful event did not exhibit facilitated eyeblink conditioning, whereas those infused with the vehicle emitted more conditioned responses than unstressed males. Females infused with muscimol before stress did not express a deficit in conditioning, whereas those infused with vehicle and stressed emitted fewer conditioned responses than unstressed vehicle controls. These data demonstrate that neuronal activity within the BLA during stress exposure is necessary to modulate learning 24 h later in a new context. Thus, the BLA is necessary to induce the long-term effect of stressful experience on conditioning regardless of sex and direction of modulation.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females

Waddell

Bangasser²,

Shors

2008

J. Neurosci.

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“…In fact, human studies show that trace eyeblink conditioning is impossible if the participant fails to verbally report the contingency of the CS and US (Clark and Squire, 1998) or severely retarded in the case of bilateral lesions of the medial temporal lobe (McGlinchey-Berroth et al, 1997). Other limbic structures, like the amygdala, have also been shown to modulate learning rate, possibly through rapidly emerging emotional associations (Neufeld and Mintz, 2001), which are seen, for example, as CSmediated reflex facilitation (e.g., Wikgren et al, 2002). Thus, the hippocampus is involved in rapidly emerging learning-related plasticity, which affects the rate at which the CR is acquired.…”

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confidence: 99%

Hippocampal Ripple-Contingent Training Accelerates Trace Eyeblink Conditioning and Retards Extinction in Rabbits

Nokia¹,

Penttonen²,

Wikgren³

2010

J. Neurosci.

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There are at least two distinct oscillatory states of the hippocampus that are related to distinct behavioral patterns. Theta (4 -12 Hz) oscillation has been suggested to indicate selective attention during which the animal concentrates on some features of the environment while suppressing reactivity to others. In contrast, sharp-wave ripples (ϳ200 Hz) can be seen in a state in which the hippocampus is at its most responsive to any kind of afferent stimulation. In addition, external stimulation tends to evoke and reset theta oscillation, the phase of which has been shown to modulate synaptic plasticity in the hippocampus. Theoretically, training on a hippocampus-dependent learning task contingent upon ripples could enhance learning rate due to elevated responsiveness and enhanced phase locking of the theta oscillation. We used a brain-computer interface to detect hippocampal ripples in rabbits to deliver trace eyeblink conditioning and extinction trials selectively contingent upon them. A yoked control group was trained regardless of their ongoing neural state. Ripplecontingent training expedited acquisition of the conditioned response early in training and evoked stronger theta-band phase locking to the conditioned stimulus. Surprisingly, ripple-contingent training also resulted in slower extinction in well trained animals. We suggest that the ongoing oscillatory activity in the hippocampus determines the extent to which a stimulus can induce a phase reset of the theta oscillation, which in turn is the determining factor of learning rate in trace eyeblink conditioning.

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“…Although there are several observations supporting its relevance to eyeblink conditioning (19)(20)(21)(22), a large part of the related molecular mechanisms are still unknown.…”

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confidence: 99%

Molecular evidence for two-stage learning and partial laterality in eyeblink conditioning of mice

Park¹,

Onodera²,

Nishimura³

et al. 2006

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

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The anterior interpositus nucleus (AIN) is the proposed site of memory formation of eyeblink conditioning. A large part of the underlying molecular events, however, remain unknown. To elucidate the molecular mechanisms, we examined transcriptional changes in the AIN of mice trained with delay eyeblink conditioning using microarray, quantitative real-time RT-PCR, and in situ hybridization techniques. Microarray analyses suggested that transcriptionally up-regulated gene sets were largely different between early (3-d training) and late (7-d) stages. Quantitative real-time RT-PCR aided by laser microdissection indicated that the expression of representative EARLY genes (Sgk, IkBa, and Plekhf1) peaked at 1-d training in both the paired and unpaired conditioning groups, and was maintained at a higher level in the paired group than in the unpaired group after 3-d training. In situ hybridization revealed increased expression of these genes in broad cerebellar areas, including the AIN, with no hemispheric preferences. In contrast, the expression of representative LATE genes (Vamp1, Camk2d, and Prkcd) was selectively increased in the AIN of the 7-d paired group, with dominance in the ipsilateral AIN. Increased Vamp1 mRNA expression was restricted to the ipsilateral dorsolateral hump, a subregion of the AIN. These expression patterns of two distinct subsets of genes fit well with the twostage learning theory, which proposes emotional and motor learning phases, and support the notion that AIN has a crucial role in memory formation of eyeblink conditioning.gene expression ͉ interpositus nucleus C lassical eyeblink conditioning is conserved among various species. Although the neuronal circuitries are well defined and the cerebellum is considered to be the site of memory formation of the classically conditioned response (CR, i.e., eyeblink) (1), evidence is still conflicting regarding the neural substrate for the memory trace of eyeblink conditioning in the cerebellum.In contrast to the suggestion that the basic memory trace of the CR is formed in the cerebellar cortex (2), accumulating evidence suggests that the anterior interpositus nucleus (AIN) in the deep cerebellar nuclei (DCN) is the site of memory for the association between the conditioned stimulus (CS) and the unconditioned stimulus (US) formed in eyeblink conditioning. This hypothesis has been examined repeatedly with lesions (3-7) and inactivation of the AIN (8, 9), and in mutant mice with Purkinje cell degeneration (10). Recent observations made using electron microscopy (11) or functional magnetic resonance imaging (12) further support the notion that the basic memory trace is formed in the AIN. On the other hand, the cerebellar cortex is implicated as a site of storage for the memory trace of CR timing (13).Although the existence of a Purkinje cell-specific promoter like L7/pcp-2 made it possible to test the relevance of some molecules to cortical function in eyeblink conditioning in vivo (14,15), mechanistic studies at the molecular level of the AIN, which is ...

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Involvement of the amygdala in classical conditioning of eyeblink response in the rat

Cited by 58 publications

References 12 publications

The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females

The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females

Hippocampal Ripple-Contingent Training Accelerates Trace Eyeblink Conditioning and Retards Extinction in Rabbits

Molecular evidence for two-stage learning and partial laterality in eyeblink conditioning of mice

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