The effects of amygdala lesions on hippocampal activity and classical eyeblink conditioning in rats

Blankenship, Matthew R.; Huckfeldt, Rachel M.; Steinmetz, Jacob J.; Steinmetz, Joseph E.

doi:10.1016/j.brainres.2004.11.061

Cited by 40 publications

(43 citation statements)

References 27 publications

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“…In line with previous research (Blankenship et al, 2005;Lee & Kim, 2004;Weisz et al, 1992) CEA lesions significantly retarded the emergence of eyeblink CRs (see Fig. 2b).…”

Section: Discussionsupporting

confidence: 93%

“…In eyeblink conditioned subjects, for instance, a number of fear CRs are observed during the first training session-before significant numbers of eyeblink CRs are produced-including autonomic changes in heart rate and blood pressure, elevated freezing, and 22 kHz ultrasonic emissions (Britton & Astheimer, 2004;Lee & Kim, 2004;Lindquist, Mahoney, & Steinmetz, 2010;Prokasy, 1972;Schneiderman, 1972). As predicted by the two-stage model, amygdala damage or pharmacological inactivation diminishes fear responding and retards eyeblink CR acquisition (Blankenship, Huckfeldt, Steinmetz, & Steinmetz, 2005;Chachich & Powell, 1998;Lee & Kim, 2004;Neufeld & Mintz, 2001;Weisz, Harden, & Xiang, 1992). No studies, to our knowledge, have reported that amygdala damage or inactivation prevents delay EBC, signifying the amygdala contributes to (but is not necessary for) the acquisition or expression of discrete motor responses.…”

mentioning

confidence: 81%

“…Based on prior EBC literature utilizing amygdala lesions or inactivation (e.g., Blankenship et al, 2005;Lee & Kim, 2004), we estimated 8 to 10 rats per group would provide sufficient power to detect significant impairments in conditioned fear and delay EBC. Approximately one week after arrival, all subjects (weighing 320-340 g) were anesthetized with respiratory isoflurane (1 %-3 %, 0.6 l/min O 2 ) and secured in a stereotaxic frame.…”

Section: Surgical Proceduresmentioning

confidence: 99%

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Central amygdala lesions inhibit pontine nuclei acoustic reactivity and retard delay eyeblink conditioning acquisition in adult rats

Pochiro

Lindquist

2015

Learn Behav

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In delay eyeblink conditioning (EBC) a neutral conditioned stimulus (CS; tone) is repeatedly paired with a mildly aversive unconditioned stimulus (US; periorbital electrical shock). Over training, subjects learn to produce an anticipatory eyeblink conditioned response (CR) during the CS, prior to US onset. While cerebellar synaptic plasticity is necessary for successful EBC, the amygdala is proposed to enhance eyeblink CR acquisition. In the current study, adult Long-Evans rats received bilateral sham or neurotoxic lesions of the central nucleus of the amygdala (CEA) followed by 1 or 4 EBC sessions. Fear-evoked freezing behavior, CS-mediated enhancement of the unconditioned response (UR), and eyeblink CR acquisition were all impaired in the CEA lesion rats relative to sham controls. There were also significantly fewer c-Fos immunoreactive cells in the pontine nuclei (PN)-major relays of acoustic information to the cerebellum-following the first and fourth EBC session in lesion rats. In sham rats, freezing behavior decreased from session 1 to 4, commensurate with nucleus-specific reductions in amygdala Fos+ cell counts. Results suggest delay EBC proceeds through three stages: in stage one the amygdala rapidly excites diffuse fear responses and PN acoustic reactivity, facilitating cerebellar synaptic plasticity and the development of eyeblink CRs in stage two, leading, in stage three, to a diminution or stabilization of conditioned fear responding.

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“…In line with previous research (Blankenship et al, 2005;Lee & Kim, 2004;Weisz et al, 1992) CEA lesions significantly retarded the emergence of eyeblink CRs (see Fig. 2b).…”

Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 81%

Section: Surgical Proceduresmentioning

confidence: 99%

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Central amygdala lesions inhibit pontine nuclei acoustic reactivity and retard delay eyeblink conditioning acquisition in adult rats

Pochiro

Lindquist

2015

Learn Behav

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“…The hippocampus exhibits morphological and excitability changes in response to stress (Galea et al, 1997;Kim et al, 2001;Shors et al, 2001) as well as eyeblink conditioning (Geinisman et al, 2001;Moyer et al, 1996). The BLA modulates neuronal activity within the hippocampus in response to stress exposure (Kim et al, 2001;Korz and Frey, 2005) and many learning tasks, including eyeblink conditioning (Pare, 2003;Huff and Rudy, 2004;Blankenship et al, 2005;McIntyre et al, 2005). The hippocampus is sensitive to fluctuating estrogen levels (Woolley et al, 1990;Yankova et al, 2001); whether estrogen levels directly influence BLA-hippocampal interactions during stress exposure and eyeblink conditioning is unknown.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, a stress-induced enhancement of contextual fear conditioning was abolished by intra-amygdala administration of the GABA agonist midazolam before stress exposure (Rodríguez Manzanares et al, 2005). 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).…”

Section: Introductionmentioning

confidence: 99%

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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Amygdala inactivation impairs eyeblink conditioning in developing rats

Freeman

2013

Developmental Psychobiology

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The amygdala facilitates acquisition of eyeblink conditioning in adult animals by enhancing conditioned stimulus (CS) inputs to the cerebellum and the unconditioned response circuitry. Ontogenetic changes in amygdala modulation of eyeblink conditioning have not been investigated directly. We examined the effects of amygdala inactivation on the ontogeny of eyeblink conditioning and conditioned freezing in rat pups. Rat pups received bilateral infusions of saline or bupivacaine into the central nucleus of the amygdala before each of the first 5 training sessions, which consisted of paired CS-US trials on postnatal days (P)17-19, P21-23, or P24-26. The final session consisted of CS-alone test trials to assess the effect of amygdala inactivation during training on conditioned freezing. Amygdala inactivation impaired acquisition of eyeblink conditioning in all of the age groups and impaired freezing to the context during the extinction test. The results indicate that the amygdala modulates cerebellar learning as soon as it begins to emerge ontogenetically.

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The effects of amygdala lesions on hippocampal activity and classical eyeblink conditioning in rats

Cited by 40 publications

References 27 publications

Central amygdala lesions inhibit pontine nuclei acoustic reactivity and retard delay eyeblink conditioning acquisition in adult rats

Central amygdala lesions inhibit pontine nuclei acoustic reactivity and retard delay eyeblink conditioning acquisition in adult rats

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

Amygdala inactivation impairs eyeblink conditioning in developing rats

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