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

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.The amygdala and the prefrontal cortex have synergistic roles in regulating purposive behavior [(Schoenbaum et al., 2000;Izquierdo and Murray, 2005); reviewed in (Barbas, 2000;Bechara et al., 2000)]. The amygdala appears to extract the affective significance of stimuli, and the prefrontal cortex guides goal-directed behavior (Damasio, 1994;Petrides, 1996;Roberts and Wallis, 2000;Levy and Goldman-Rakic, 2000;Fuster, 2000;Barbas et al., 2002). Communication between the amygdala and the prefrontal cortex is bidirectional [e.g., (Nauta, 1961;Pandya et al., 1973;Jacobson and Trojanowski, 1975;Aggleton et al., 1980;Porrino et al., e Current address: Department of Molecular Biomedical Sciences, School of Veterinary Medicine, North Carolina State University, Raleigh, NC. * Corresponding author. Dept. Health Sciences, Boston University, 635 Commonwealth Ave. Room 431, Boston, MA 02215. E-mail address: barbas@bu.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is p...

Effects of neonatal amygdala or hippocampus lesions on resting brain metabolism in the macaque monkey: A microPET imaging study

“…Each of these cortical and subcortical regions has substantial connections with the amygdala, especially the lateral, basal and accessory basal nuclei (Amaral et al, 1992, Stefanacci and Amaral, 2000, Shelton et al, 2002, Ghashghaei et al, 2007. These results also parallel a recent autoradiography study of cerebral glucose metabolism in adult rats that received ibotenic acid amygdala lesions as neonates (Gerrits et al, 2006).…”

“…First, amygdala-lesioned animals displayed hypometabolism in the dorsolateral prefrontal cortex, an area with which the amygdala shares only light connections (Amaral et al, 1992, Ghashghaei et al, 2007. However, other evidence points to a stronger functional relationship between the medial temporal lobe and the prefrontal cortex.…”

“…Although the amygdala does not share any direct, monosynaptic connections with the cerebellum in nonhuman primates, the recent use of rabies virus as a transneuronal anatomical tracer has indicated multi-synaptic connections between the cerebellum and the prefrontal cortex (especially the dorsolateral prefrontal cortex, Kelly and Strick, 2003), and also between the cerebellum and putamen (Hoshi et al, 2005). It is possible that neonatal amygdala damage could influence metabolism in the cerebellum through these intermediary structures, since the amygdala possesses light, bidirectional connections with the dorsolateral prefrontal cortex and unidirectional connections with the putamen (Amaral et al, 1992, Ghashghaei et al, 2007, and both were significantly hypometabolic for amygdalalesioned animals.Is it possible that the cerebellar hypermetabolism is an artifact of the microPET normalization process? Forcing all microPET datasets to have an equal whole brain mean RI count was necessary to control for differential uptake of [ 18 F]FDG across animals.…”

Mindfulness and emotion regulation—an fMRI study

“…On the neurobiological level, cognitive emotion regulation studies find regulatory influences of prefrontal top-down inhibitory structures, such as the dorsolateral and ventrolateral prefrontal cortex (DLPFC, VLPFC) and the dorsomedial prefrontal cortex (DMPFC), on bottom-up emotion propagating structures, such as the amygdala (recent reviews: Kalisch, 2009;Diekhof et al, 2011;Kanske et al, 2011;selected studies: Beauregard et al, 2001;Ochsner et al, 2002;Urry et al, 2006;Banks et al, 2007;Herwig et al, 2007b). The notion of top-down regulatory influences of prefrontal regions on amygdala is further supported by tracing and stimulation studies in animals (Ghashghaei et al, 2007;Quirk, 2007).…”

Structural and functional neural correlates of a mind-body connection.

“…Although there were hemispheric differences in these findings -left ACC and left UF in contrast to the right amygdala -these three structures nonetheless comprise a frontolimbic network that is involved in regulating emotion and reward processing (Bush et al 2000;Botvinick et al, 2004;Etkin et al 2006;Petrides & Pandya, 2007;Ghashghaei et al, 2007;Wang et al, 2009). More specifically, the ACC and subgenual regions that are considered the vmPFC send projections to the amygdala through the UF.…”