The medial geniculate, not the amygdala, as the root of auditory fear conditioning

Abstract

The neural basis of auditory fear conditioning (AFC) is almost universally believed to be the amygdala, where auditory fear memories are reputedly acquired and stored. This widely-accepted amygdala model holds that that the auditory conditioned stimulus (CS) and the nociceptive unconditioned stimulus (US) first converge in the lateral nucleus of the amygdala (AL), and are projected independently to it from the medial division of the medial geniculate nucleus (MGm) and the adjacent posterior intralaminar nucleus (PIN), which serve merely as sensory relays. However, the four criteria that are used to support the AL model, (a) CS-US convergence, (b) associative plasticity, (c) LTP and (d) lesion-induced learning impairment, are also met by the MGm/PIN. Synaptic and molecular approaches supporting the AL also implicate the MGm/PIN. As both the AL and its preceding MGm/PIN are critically involved, we propose that the latter be considered the "root" of AFC.

Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal

“…40), as also evident from human neuroimaging studies using a variety of sensory stimuli (41,42). The medial geniculate nucleus may work in concert with the amygdala for auditory fear conditioning (43).…”

“…Finally, influences from the amygdala to auditory cortex are known to be cholinergically mediated (via nucleus basalis; e.g., ref. 43), raising the intriguing possibility of applying pharmacological manipulations (10,(51)(52)(53) to our human MEG paradigm in future work.…”

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

“…One view posits that thalamic and cortical neurons transmitting CS information to LA merely serve as sensory relays. Another stipulates that thalamic and/or cortical plasticity is critical for fear conditioning (for review, see Weinberger 2011). Thus, we first examined whether our model could reproduce the findings of Repa et al (2001) when the CS responsiveness of thalamic and cortical neurons relaying tone information to LAd remained unchanged at 20 Hz (habituation level) through conditioning.…”

“…The experimental paradigm typically used to study this process is Pavlovian fear conditioning, where an initially neutral stimulus (conditioned stimulus [CS]) acquires the ability to elicit conditioned fear responses after pairing with a noxious unconditioned stimulus (US). Although there is evidence that fear conditioning induces widespread synaptic plasticity in the brain, including at thalamic and cortical levels (Letzkus et al 2011;Weinberger 2011), there are also data indicating that the dorsal portion of the lateral amygdala (LAd) is a critical site of plasticity for the storage of CS -US associations (LeDoux 2000; for review, see Pape and Paré 2010).…”

“…Similarly, although it is well established that fear conditioning increases the CS responsiveness of thalamic and cortical neurons projecting to LA (for review, see Weinberger 2011), the contributions of CS afferent pathways to conditioned fear memories remain controversial. In particular, it has been impossible to determine the relative importance of plasticity within LA vs. CS inputs to LA.…”