Elsevier

Neuroscience

Volume 115, Issue 4, 16 December 2002, Pages 1261-1279
Neuroscience

Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey

https://doi.org/10.1016/S0306-4522(02)00446-3Get rights and content

Abstract

The amygdala has been implicated in processing information about the emotional significance of the environment and in the expression of emotions, through robust pathways with prefrontal, anterior temporal areas, and central autonomic structures. We investigated the anatomic organization and intersection of these pathways in the amygdala in rhesus monkeys with the aid of bidirectional, retrograde and anterograde tracers. Connections of the amygdala with orbitofrontal and medial prefrontal areas were robust and bidirectional, whereas connections with lateral prefrontal areas were sparse, unidirectional and ascending. Orbitofrontal axons terminated densely in a narrow band around the borders of the magnocellular basolateral nucleus, surrounded by projection neurons along a continuum through the nuclei of the basal complex. In contrast, the input and output zones of medial prefrontal areas were intermingled in the amygdala. Moreover, medial prefrontal axonal terminations were expansive, spreading into the parvicellular basolateral nucleus, which is robustly connected with hypothalamic autonomic structures, suggesting that they may influence the expressive emotional system of the amygdala. On the other hand, orbitofrontal axons heavily targeted the intercalated masses, which issue inhibitory projections to the central nucleus, at least in rats and cats. The central nucleus, in turn, issues a significant inhibitory projection to hypothalamic and brainstem autonomic structures. This evidence suggests that orbitofrontal areas exercise control on the internal processing of the amygdala. In addition, the results provided direct evidence that the connections of anterior temporal visual and auditory association cortices occupy overlapping territories with the orbitofrontal cortices particularly in the posterior half of the amygdala, and specifically within the intermediate sector of the basolateral nucleus and in the magnocellular part of the basomedial nucleus (also known as accessory basal), suggesting a closely linked triadic network. This intricate network may be recruited in cognitive tasks that are inextricably linked with emotional associations.

Section snippets

Surgical procedures

Experiments were conducted on 26 rhesus monkeys (Macaca mulatta), obtained through the Washington and New England Regional Primate Research Centers. Experiments were conducted according to the NIH guide for the Care and Use of Laboratory Animals (NIH publication 86-23, revised 1987), and all efforts were made to minimize animal suffering and to reduce their number. The monkeys were anesthetized with ketamine hydrochloride (10–15 mg/kg, intramuscularly) followed by sodium pentobarbital

Injection sites and neural tracers

Results were obtained from experiments with injections of neural tracers in several prefrontal cortices, and in a sample of anterior temporal areas, and autonomic hypothalamic structures, both linked with the amygdala as well as with prefrontal cortices. A composite diagram of the location of tracer injections is shown in Fig. 1, and the cases, types of dyes used, injection sites and hemisphere, and analyses conducted are presented in Table 1. Details for most injection sites in prefrontal

Partly segregated input–output zones link the amygdala with orbitofrontal cortices

There is strong evidence that the amygdala and the orbitofrontal cortex have an important role in emotions (for reviews see Kling and Steklis, 1976, Aggleton, 1993, Damasio, 1994, Davis, 1997, Roberts and Wallis, 2000, Rolls, 2000, Bechara et al., 2000, Elliott et al., 2000, LeDoux, 2000). Our results indicated that the circuits connecting these structures are bidirectional, suggesting a strong functional tie. Moreover, the connections have spatially distinct input and output zones.

Conclusion

The unique role of the amygdala and the orbitofrontal cortex in emotions is not understood. The amygdala increases its activity when viewing masked fearful faces, when there is no awareness of the event (Whalen et al., 1998). Moreover, a subcortical loop connecting the amygdala with the thalamus can support fear conditioning (Romanski and LeDoux, 1992). Since the experience of emotions likely involves the cortex (Kennard, 1945), the robust bidirectional pathways linking the amygdala with

Acknowledgements

We thank Ms. Karen Trait for help with immunocytochemical assays, Dr. Ron Killiany for assistance with MR imaging, and Dr. Deepak Pandya for the autoradiographic cases. This work was supported by grants from NIH (NIMH and NINDS).

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