Abstract

Studies on the thalamus have mostly focused on sensory relay nuclei, but the organization of pathways associated with emotions is not well understood. We addressed this issue by testing the hypothesis that the primate amygdala acts, in part, like a sensory structure for the affective import of stimuli and conveys this information to the mediodorsal thalamic nucleus, magnocellular part (MDmc). We found that primate sensory cortices innervate amygdalar sites that project to the MDmc, which projects to the orbitofrontal cortex. As in sensory thalamic systems, large amygdalar terminals innervated excitatory relay and inhibitory neurons in the MDmc that facilitate faithful transmission to the cortex. The amygdala, however, uniquely innervated a few MDmc neurons by surrounding and isolating large segments of their proximal dendrites, as revealed by three-dimensional high-resolution reconstruction. Physiologic studies have shown that large axon terminals are found in pathways issued from motor systems that innervate other brain centers to help distinguish self-initiated from other movements. By analogy, the amygdalar pathway to the MDmc may convey signals forwarded to the orbitofrontal cortex to monitor and update the status of the environment in processes deranged in schizophrenia, resulting in attribution of thoughts and actions to external sources.

Highlights

  • The amygdala has a key role in sensing the significance of stimuli and events, but the organization of pathways that enable this vital function is not well understood

  • The upper layer projection from sensory association cortices to the amygdala is akin to the pattern seen in feedforward pathways that link earlier-processing with later-processing sensory areas in cortex [16]

  • The amygdalar boutons in MDmc were distinguished for their large size, being on average 2.5 times larger in their major diameter than boutons in the midline nuclei

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Summary

Introduction

The amygdala has a key role in sensing the significance of stimuli and events, but the organization of pathways that enable this vital function is not well understood. The pathway connecting the amygdala with the MDmc remains largely unexplored at the synaptic level in primates, and even its organization at the level of the system is not well understood We addressed both issues from the system to the synapse for the amygdalar projection to the MDmc and compared it to the classical triads described for the pathway from the retina to the dorsal lateral geniculate nucleus (LGN) in rhesus monkeys. We found novel, to our knowledge, complex, and unusually strong synaptic interactions of amygdalar pathways in the MDmc that appear to be unique to this system These findings attest to the significance of the amygdalar pathways for the synthesis of cognitive and emotional processes for action

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