Amygdalostriatal projections in the neurocircuitry for motivation: a neuroanatomical thread through the career of Ann Kelley

Abstract

In MacLean’s triune brain, the amygdala putatively subserves motivated behavior by modulating the “reptilian” basal ganglia. Accordingly, Ann Kelley, with Domesick and Nauta, influentially showed that amygdalostriatal projections are much more extensive than were appreciated. Caudal of the anterior commissure, the entire striatum receives afferents from deep basal nuclei of the amygdala. They highlighted that amygdalar projections to the rostral ventromedial striatum converged with projections from the ventral tegmental area and cingulate cortex, forming a “limbic striatum”. Orthologous topographic projections subsequently were observed in fish, amphibians, and reptiles. Subsequent functional studies linked acquired value to action via this neuroanatomical substrate. From Dr. Kelley’s work evolved insights into components of the distributed, interconnected network that subserves motivated behavior, including the nucleus accumbens shell and core and the striatal-like extended amygdala macrostructure. These heuristic frameworks provide a neuroanatomical basis for adaptively translating motivation into behavior. The ancient amygdala-to-striatum pathways remain a current functional thread not only for stimulus–response valuation, but also for the psychopathological plasticity that underlies addictionrelated memory, craving and relapse.

Attention as an effect not a cause

“…The striatum receives converging inputs from many sources, prominently from the cerebral cortex, but also from the thalamus, amygdala, and elsewhere [21-24]. The striatum also receives dopamine signals that guide reinforcement learning; the learned associations between a particular state and the set of actions with the highest expected values establish a decision policy that then guides the subject’s behavior [25-29].…”

Serotonin and stress coping

“…Indeed, the NAc Shell receives relevant functional inputs from the BLA ( [134], for a recent review) and manipulation of local GABAergic circuits or of glutamatergic (GLU) inputs in the caudal portion of the NAc Shell elicits defensive responses in the rat, including anti-predator treading and bites aimed at the experimenter [135]. On the other hand, there is convincing evidence that stressful experiences powerfully modulate dopamine (DA) tonic levels in the NAc Shell and that increased DA tone in this brain area mediates expression of active coping responses, whereas low DA tone is associated with behavioral indices of helplessness [6,136], in processes also involving DA receptors and glutamate transmission [137,138].…”

Neuroimaging as a biomarker in symptom validity and performance validity testing

“…Likewise, the Bmotivation^construct was a critical element of learning theory during that era (Kimble 1950). Motivational factors, as they should, remain key to understanding human behavior today, but with a much greater focus on the neurobiology of motivation than in the past (Arnsten and Rubia 2012;Robinson et al 2014;Zorrilla and Koob 2013).…”