Elsevier

NeuroImage

Volume 34, Issue 3, 1 February 2007, Pages 905-923
NeuroImage

Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala

https://doi.org/10.1016/j.neuroimage.2006.09.046Get rights and content

Abstract

The prefrontal cortex and the amygdala have synergistic roles in regulating purposive behavior, effected through bidirectional pathways. Here we investigated the largely unknown extent and laminar relationship of prefrontal input–output zones linked with the amygdala using neural tracers injected in the amygdala in rhesus monkeys. Prefrontal areas varied vastly in their connections with the amygdala, with the densest connections found in posterior orbitofrontal and posterior medial cortices, and the sparsest in anterior lateral prefrontal areas, especially area 10. Prefrontal projection neurons directed to the amygdala originated in layer 5, but significant numbers were also found in layers 2 and 3 in posterior medial and orbitofrontal cortices. Amygdalar axonal terminations in prefrontal cortex were most frequently distributed in bilaminar bands in the superficial and deep layers, by columns spanning the entire cortical depth, and less frequently as small patches centered in the superficial or deep layers. Heavy terminations in layers 1–2 overlapped with calbindin-positive inhibitory neurons. A comparison of the relationship of input to output projections revealed that among the most heavily connected cortices, cingulate areas 25 and 24 issued comparatively more projections to the amygdala than they received, whereas caudal orbitofrontal areas were more receivers than senders. Further, there was a significant relationship between the proportion of ‘feedforward’ cortical projections from layers 2–3 to ‘feedback’ terminations innervating the superficial layers of prefrontal cortices. These findings indicate that the connections between prefrontal cortices and the amygdala follow similar patterns as corticocortical connections, and by analogy suggest pathways underlying the sequence of information processing for emotions.

Section snippets

Materials and methods

Experiments were conducted on 4 adult rhesus monkeys (Macaca mulatta) of both sexes, obtained through the New England Regional Primate Research Center (NEPRC). Experiments were conducted according to the NIH guide for the Care and Use of Laboratory Animals (NIH publication 86–23, revised 1987). Experimental methods and euthanasia were approved by the IACUC at NEPRC, Harvard Medical School, and Boston University School of Medicine. All efforts were made to minimize animal suffering and to reduce

Injection sites

In one group of experiments (n = 3) retrograde fluorescent tracers occupied restricted sites of the basal nuclei of the amygdala (Figs. 1B–D, Table 1). In a second group of experiments (n = 4 hemispheres) the bidirectional tracer BDA occupied extensive parts of the basal complex of the amygdala (Figs. 1A–B; D–F; A′–E′). In all cases, labeled projection neurons and axonal terminals were found in nearly all prefrontal areas, but varied in density in areas and distinct layers, as elaborated below.

Prefrontal projection neurons directed to the amygdala

Discussion

Caudal orbitofrontal and anterior cingulate areas had the strongest connections with the amygdala, confirming previous studies (Porrino et al., 1981, Amaral and Price, 1984). The present findings further indicate that prefrontal connections with the amygdala were more extensive than previously thought, extending beyond the most heavily linked orbitofrontal and medial cingulate cortices, described previously for primates and rats (Nauta, 1961, Jacobson and Trojanowski, 1975, Porrino et al., 1981

Acknowledgments

We thank Dr. Ron Killiany for help with brain imaging and Ms. Karen Trait for technical assistance. Research was supported by NIH grants from NIMH and NINDS.

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    1

    Current address: Department of Molecular Biomedical Sciences, School of Veterinary Medicine, North Carolina State University, Raleigh, NC, USA.

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