Ltp May Equal Memory In The Amygdala

In 1997, two groups broke through a long-standing barrier by directly demonstrating the occurrence of LTP in association with behavioral training in animals (55, 56). Thus, the amygdala became the envy of hippocampologists everywhere. These studies were particularly compelling because in this system there is appreciable understanding of the structure of the relevant circuits and how they map onto the behavior (see Panel A).

The behavioral system under study by both groups was cued fear conditioning, which we discussed as a popular rodent learning paradigm in Chapter 2. In this paradigm, the animal learns to associate an auditory cue (the CS) with an aversive foot shock (the US). The US normally elicits a spectrum of defensive, fear-associated behaviors such as immobile posture (freezing), tachycardia, and increased respiration— these are the unconditioned response (UR). As with all associative learning, after CS-US pairing the CS becomes enabled to elicit the UR, and after fear-conditioning training, the auditory cue elicits the same spectrum of defensive and physiologic responses as the foot shock did previously.

The relevant pathways involve the amygdala. The tone CS is transduced to the lateral nucleus of the amygdala via both thalamic and cortical relays (see Panel A). The shock pathway also triggers activity in the lateral nucleus via a strong input, the pathway that mediates triggering the reflex defensive behaviors. Pairing of the cue with the US somehow allows the CS to co-opt the reflex pathway and trigger the defensive responses on its own.

How does this happen? Pat Shinnick-Gallagher's group and Joe LeDoux's group have both performed experiments indicating that pairing of the strong US signal with the weaker CS input to the lateral nucleus of the amygdala leads to LTP of the CS input (55-57). This LTP results in the augmentation or unmasking of a latent circuit—the CS is now able to trigger the entire spectrum of defensive behaviors because the CS input is now sufficiently strong (Panel A, right half). This strong CS input is able to activate the lateral nucleus cells and trigger the conditioned response.

The key findings by both groups involved directly measuring LTP production in the amygdala in response to behavioral training. The two groups took distinct and complementary approaches to looking for LTP in response to fear conditioning training. McKernan and Shinnick-Gallagher used an ex vivo approach (55). These investigators trained animals and assessed the presence of LTP in amygdala slices prepared acutely, using electrical stimulation of synaptic inputs to the lateral nucleus from the medial geniculate nucleus (see Panel B). LeDoux's colleagues used in vivo recording techniques with implanted electrodes (see Panel C and reference 56). They monitored field responses from the amygdala in response to presentation of the tone cue—directly monitoring population neuronal responses to an environmental signal. Both approaches yielded the same conclusion—synaptic potentiation of CS inputs into the amygdala is occurring with fear-conditioning training.

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