Heterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala

Bauer, Elizabeth P.; LeDoux, Joseph E.

doi:10.1523/jneurosci.3567-04.2004

Cited by 98 publications

(91 citation statements)

References 46 publications

(68 reference statements)

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“…Local circuit GABAergic interneurons in the LA provide substantial feedforward and feedback inhibition that not only controls their activity (Li et al, 1996;Lang and Pare, 1997;Woodruff and Sah, 2007a,b) but also acts as a brake on plasticity of glutamatergic inputs to principal neurons (Bissiere et al, 2003). Cortical inputs to some interneurons in the rat LA also show synaptic plasticity (Mahanty and Sah, 1998;Bauer and LeDoux, 2004). However, neither the identity of these interneurons nor the mechanisms that underlie this LTP is known.…”

Section: Resultsmentioning

confidence: 99%

A Specific Class of Interneuron Mediates Inhibitory Plasticity in the Lateral Amygdala

Polepalli

Sullivan²,

Yanagawa³

et al. 2010

J. Neurosci.

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The lateral amygdala (LA) plays a key role in emotional learning and is the main site for sensory input into the amygdala. Within the LA, pyramidal neurons comprise the major cell population with plasticity of inputs to these neurons thought to underlie fear learning. Pyramidal neuron activity is tightly controlled by local interneurons, and GABAergic modulation strongly influences amygdaladependent learning. Synaptic inputs to some interneurons in the LA can also undergo synaptic plasticity, but the identity of these cells and the mechanisms that underlie this plasticity are not known. Here we show that long-term potentiation (LTP) in LA interneurons is restricted to a specific type of interneuron that is defined by the lack of expression of synaptic NR2B subunits. We find that LTP is only present at cortical inputs to these cells and is initiated by calcium influx via calcium-permeable AMPA receptors. LTP is maintained by trafficking of GluR2-lacking AMPA receptors that require an interaction with SAP97 and the actin cytoskeleton. Our results define a novel population of interneurons in the LA that control principal neuron excitability by feed-forward inhibition of cortical origin. This selective enhanced inhibition may contribute to reducing the activity of principal neurons engaged during extinction of conditioned fear.

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Section: Resultsmentioning

confidence: 99%

A Specific Class of Interneuron Mediates Inhibitory Plasticity in the Lateral Amygdala

Polepalli

Sullivan²,

Yanagawa³

et al. 2010

J. Neurosci.

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“…Induction of LTP at thalamic and cortical inputs to principal cells has been found to depend on postsynaptic depolarization allowing influx of Ca 2+ ions via NMDA receptors (Bauer et al 2002;Tsvetkov et al 2002) and/or voltagedependent L-type Ca 2+ channels (Weisskopf et al 1999;Bauer et al 2002;Humeau et al 2005). In addition, it was reported that excitatory glutamatergic synapses from the thalamus or cortex onto interneurons exhibit NMDA-receptor-dependent potentiation (Bauer and LeDoux 2004). This potentiation is also AMPA-receptor-dependent because AMPA receptors on inhibitory neurons lack the GluR2 subunit, making them calcium-permeable (Mahanty and Sah 1998).…”

Section: Activity-dependent Synaptic Plasticitymentioning

confidence: 99%

“…This potentiation is also AMPA-receptor-dependent because AMPA receptors on inhibitory neurons lack the GluR2 subunit, making them calcium-permeable (Mahanty and Sah 1998). It was further shown that inhibitory inputs onto pyramidal cells are modifiable via a Ca 2+ -dependent mechanism (Bauer and LeDoux 2004). In addition to LTP, longterm depression (LTD) can be readily induced at excitatory amygdala synapses by low-frequency stimulation of the lateral nucleus at 1 Hz for 15 min (Wang and Gean 1999).…”

Section: Activity-dependent Synaptic Plasticitymentioning

confidence: 99%

Mechanisms contributing to the induction and storage of Pavlovian fear memories in the lateral amygdala

2013

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The relative contributions of plasticity in the amygdala vs. its afferent pathways to conditioned fear remain controversial. Some believe that thalamic and cortical neurons transmitting information about the conditioned stimulus (CS) to the lateral amygdala (LA) serve a relay function. Others maintain that thalamic and/or cortical plasticity is critically involved in fear conditioning. To address this question, we developed a large-scale biophysical model of the LA that could reproduce earlier findings regarding the cellular correlates of fear conditioning in LA. We then conducted model experiments that examined whether fear memories depend on (1) training-induced increases in the responsiveness of thalamic and cortical neurons projecting to LA, (2) plasticity at the synapses they form in LA, and/or (3) plasticity at synapses between LA neurons. These tests revealed that training-induced increases in the responsiveness of afferent neurons are required for fear memory formation. However, once the memory has been formed, this factor is no longer required because the efficacy of the synapses that thalamic and cortical neurons form with LA cells has augmented enough to maintain the memory. In contrast, our model experiments suggest that plasticity at synapses between LA neurons plays a minor role in maintaining the fear memory.

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“…This DA-dependency is due in part to a DA modulation of the plastic synaptic events that underlie reinforcement and associative learning. Synaptic plasticity has indeed been shown to occur at target structures of the VTA, including the NAc (Kombian and Malenka 1994;Li and Kauer 2004;Pennartz et al 1993;Robbe et al 2002;Taverna and Pennartz 2003;Thomas et al 2001), PFC (Otani et al 2003) and amygdala (Bauer and LeDoux 2004;Bauer et al 2002;Fourcaudot et al 2009;Kandel 1998, 2007;Humeau et al 2003;Samson and Pare 2005). DA was shown to modulate plasticity in the striatum (Calabresi et al 2007;Centonze et al 2003;Kerr and Wickens 2001;Pawlak and Kerr 2008;Reynolds et al 2001), the amygdala (Bissière et al 2003), PFC Kolomiets et al 2009) and hippocampus (Frey et al 1989(Frey et al , 1990(Frey et al , 1991Lisman 1996, 1998;Gurden et al 1999) but not in the NAc.…”

Section: Models Of the Effects Of Dopamine Releasementioning

confidence: 99%

Computational models of reinforcement learning: the role of dopamine as a reward signal

2010

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Reinforcement learning is ubiquitous. Unlike other forms of learning, it involves the processing of fast yet content-poor feedback information to correct assumptions about the nature of a task or of a set of stimuli. This feedback information is often delivered as generic rewards or punishments, and has little to do with the stimulus features to be learned. How can such low-content feedback lead to such an efficient learning paradigm? Through a review of existing neuro-computational models of reinforcement learning, we suggest that the efficiency of this type of learning resides in the dynamic and synergistic cooperation of brain systems that use different levels of computations. The implementation of reward signals at the synaptic, cellular, network and system levels give the organism the necessary robustness, adaptability and processing speed required for evolutionary and behavioral success.

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Heterosynaptic Long-Term Potentiation of Inhibitory Interneurons in the Lateral Amygdala

Cited by 98 publications

References 46 publications

A Specific Class of Interneuron Mediates Inhibitory Plasticity in the Lateral Amygdala

A Specific Class of Interneuron Mediates Inhibitory Plasticity in the Lateral Amygdala

Mechanisms contributing to the induction and storage of Pavlovian fear memories in the lateral amygdala

Computational models of reinforcement learning: the role of dopamine as a reward signal

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