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

Abstract

AbstractöThe amygdala has been implicated in processing information about the emotional signi¢cance 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 in£uence 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 signi¢cant 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 speci¢cally 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.

Dissociable relations between amygdala subregional networks and psychopathy trait dimensions in conduct‐disordered juvenile offenders

“…These intrinsic brain networks are relatively stable across participants and time [Smith et al, 2009], correspond spatially with well‐known functional networks [Smith et al, 2009], and can signal abnormal brain function and psychopathology [Greicius, 2008]. Employing iFC analysis, dissociable BLA and CMA connectivity profiles were recently documented in healthy adults and adolescents [Gabard‐Durnam et al, 2014; Qin et al, 2012; Roy et al, 2009], consistent with animal models of amygdaloid circuitry [Ghashghaei and Barbas, 2002; Keifer et al, 2015; LeDoux, 2007; Pessoa, 2011; Sah et al, 2003]. Further echoing earlier animal work, these iFC profiles were shown to undergo extensive age‐dependent changes, with BLA and CMA connectivity becoming increasingly segregated and specialized during the transition from adolescence to adulthood [Qin et al, 2012].…”

“…Within this system, posterolateral parietal regions seem to orient attention in time and space and are necessary for conscious perception, while lateral and medial prefrontal areas seemingly accommodate task‐driven attention modulation and response selection, along with cognitive and behavioral control of action [Arnsten and Rubia, 2012; Menon, 2011; Seeley et al, 2007]. Whereas lateral divisions within parietal and prefrontal cortices have sparse amygdalar connections [Amaral and Price, 1984; Leichnetz, 2001; Selemon and Goldmanrakic, 1988], medial prefrontal areas are richly and reciprocally connected to BLA neurons [Barbas et al, 2003; Ghashghaei and Barbas, 2002; Sah et al, 2003; Selemon and Goldmanrakic, 1988], and thus allow potential BLA‐frontoparietal interactions. Importantly, most frontoparietal system components exhibit BLA functional connectivity during task performance and at rest [Bzdok et al, 2013; Pessoa, 2011; Qin et al, 2012], further supporting the notion of reciprocal interactions.…”

“…Excessive frontoparietal control of BLA neurons and diminished BLA responding have been tentatively theorized in relation to impulsive and antisocial psychopathic traits [Blair, 2010; Blair, 2013b; Blair and Mitchell, 2009; Glenn et al, 2009; Larson et al, 2013; Moul et al, 2012], and subsumed to underpin the executive dysfunction and behavioral disinhibition that lie at the heart of these traits [Dolan and Anderson, 2002; Morgan and Lilienfeld, 2000; Racer et al, 2011; Sadeh and Verona, 2008; Sellbom and Verona, 2007; Zeier et al, 2012]. However, given the bidirectional flow of information between the BLA and frontoparietal structures [Barbas et al, 2003; Ghashghaei and Barbas, 2002; Sah et al, 2003; Selemon and Goldmanrakic, 1988], our finding may also reflect exaggerated bottom‐up signaling of motivational salience, potentially at the expense of negative emotional information. This fits well with the neurocognitive profile of behavioral psychopathic traits, which includes excessive deployment of cognitive resources towards positive and motivationally salient information [Dolan and Anderson, 2002; Morgan and Lilienfeld, 2000; Racer et al, 2011; Sadeh and Verona, 2008; Sellbom and Verona, 2007], and is consistent with the role of BLA in processing motivational salience [Dwyer and Killcross, 2006; Tye and Janak, 2007].…”

“…The BLA receives information from multiple brain systems and is a site of integration with cortical territories, including those that regulate socioemotional functions [Bzdok et al, 2013; Ghashghaei and Barbas, 2002; LeDoux, 2007; Pessoa, 2011; Sah et al, 2003]. It contributes greatly to the perception, evaluation, and memory formation of emotionally salient events [Davis and Whalen, 2001; LeDoux, 2007; Moul et al, 2012].…”

“…It contributes greatly to the perception, evaluation, and memory formation of emotionally salient events [Davis and Whalen, 2001; LeDoux, 2007; Moul et al, 2012]. The CMA, in contrast, is less heavily integrated with cortical circuits, though its thalamic and insular connections do allow for cortical crosstalks that seemingly shape early information processing [Bienkowski and Rinaman, 2013; Bzdok et al, 2013; Ghashghaei and Barbas, 2002; Keifer et al, 2015; Pessoa, 2011; Sah et al, 2003]. It is the primary output site of the amygdala, and orchestrates behavioral and physiological aspects of emotion processing and associative learning via its projections to the brainstem, cerebellum, and hypothalamus [Davis and Whalen, 2001; LeDoux, 2007; Moul et al, 2012].…”