A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes

doi:10.1016/j.neubiorev.2008.10.009

Neuroscience & Biobehavioral Reviews

Volume 33, Issue 3, March 2009, Pages 367-382

https://doi.org/10.1016/j.neubiorev.2008.10.009 Get rights and content

Abstract

Adolescence is the transition period that prepares individuals for fulfilling their role as adults. Most conspicuous in this transition period is the peak level of risk-taking behaviors that characterize adolescent motivated behavior. Significant neural remodeling contributes to this change. This review focuses on the functional neuroanatomy underlying motivated behavior, and how ontogenic changes can explain the typical behavioral patterns in adolescence. To help model these changes and provide testable hypotheses, a neural systems-based theory is presented. In short, the Triadic Model proposes that motivated behavior is governed by a carefully orchestrated articulation among three systems, approach, avoidance and regulatory. These three systems map to distinct, but overlapping, neural circuits, whose representatives are the striatum, the amygdala and the medial prefrontal cortex. Each of these system-representatives will be described from a functional anatomy perspective that includes a review of their connectivity and what is known of their ontogenic changes.

Section snippets

Introduction to adolescence

Adolescence is the transition period during which individuals acquire and refine cognitive, emotional, and social skills in preparation for their ultimate role as responsible, independent and sexually mature adults. This period is marked by typical physical and behavioral changes. These changes result from an interplay of biological and environmental factors. The biological factors arise from the genetic, hormonal and neural domains. These factors promote changes that occur along a set timeline

Neural systems models

A number of greatly influential theories of prefrontal cortical function have been proposed in an effort to understand the mechanisms underlying complex behavior (to cite a few, Dehaene and Changeux, 1997, Duncan, 2001, Fuster, 1997, Goldman-Rakic, 1998, Grafman, 2002, Miller and Cohen, 2001, Rolls, 1996, Shallice and Burgess, 1996, Sigman and Dehaene, 2008). For example, Baddeley (2000) proposed a model of working memory that recognized two main functional components ‘holding stimuli online’

The Triadic Model

Prior to describing the model, the term motivated behavior needs clarification. Indeed, a variety of terms are used in the literature to refer to motivated behavior. Such terms include ‘goal-directed behavior’, ‘conscious behavior’, or ‘decision-making’, to cite only a few. To avoid confusion, we will use selectively the term ‘motivated behavior’, which we define operationally as actions taken in response to stimuli to achieve a goal. Schematically, two sets of behaviors can be generated in

Anatomy and connectivity

The amygdala is a complex structure composed of highly interconnected nuclei that resides in the anterior temporal lobe (Price and Russchen, 1987) (Fig. 2). These nuclei can be functionally distinguished based on gene expression patterns, which correlate with unique embryologic origins (Zirlinger et al., 2001). They also have unique sets of interconnections with one another (Amaral et al., 1992; Pitkanen et al., 2003). We describe the general organization of the amygdala subregions and

Conclusion

In summary, this review underscores the complexity of the anatomical and functional organization of key structures underlying motivated behavior. Most notably, it provides a template along which to coordinate future research on the role of these structures and associated systems in the control of behavior.

The Fractal Triadic Model is ideally suited for the study of ontogenic neural changes and their consequences on behavior, as evidenced by the emerging functional neuroimaging studies of reward

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Published by Elsevier Ltd.

ReviewA developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes

Abstract

Section snippets

Introduction to adolescence

Neural systems models

The Triadic Model

Anatomy and connectivity

Conclusion

Neurosci. Biobehav. Rev.

Trends Neurosci.

Neuroscience

Dev. Rev.

Neuropsychologia

Trends Cogn. Sci.

Neuroscience

Neuron

Trends Neurosci.

Neuroscience

Neurosci. Biobehav. Rev.

Neuron

Neuron

Neurosci. Biobehav. Rev.

Neuroscience

Neuropsychologia

J. Am. Acad. Child Adolesc. Psychiatry

Int. Rev. Neurobiol.

Neuroimage

Biol. Psychiatry

Cognition

Neuroscience

Neuroscience

Neuroscience

Neuropsychologia

Neuroscience

Behav. Brain Res.

Trends Neurosci.

Brain Res.

Behavioral symptoms after pallido-nigral lesions: a clinico-pathological case

Neurocase

A mechanism for impaired fear recognition after amygdala damage

Nature

Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

Nature

Fear and the human amygdala

J. Neurosci.

The functional effects of amygdala lesions in humans: a comparison with findings from monkeys

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

Extended amygdala and basal forebrain

Ann. N. Y. Acad. Sci.

Amygdalohippocampal and amygdalocortical projections in the primate brain

Adv. Exp. Med. Biol.

Anatomical organization of the primate amygdaloid complex

Meeting of minds: the medial frontal cortex and social cognition

Nat. Rev. Neurosci.

The development of mother-infant interactions after neonatal amygdala lesions in rhesus monkeys

J. Neurosci.

Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

J. Neurosci.

Decision-making and impulse control after frontal lobe injuries

Curr. Opin. Neurol.

Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood

Arch. Gen. Psychiatry

Newly generated neurons in the amygdala and adjoining cortex of adult primates

Proc. Natl. Acad. Sci. U.S.A.

Amygdala contribution to selective dimensions of emotion

Soc. Cogn. Affect Neurosci.

Incentive-elicited brain activation in adolescents: similarities and differences from young adults

J. Neurosci.

Doing without schema hierarchies: a recurrent connectionist approach to normal and impaired routine sequential action

Psychol. Rev.

Cytodifferentiation and synaptogenesis in the neostriatum of fetal and neonatal rhesus monkeys

Anat. Embryol. (Berl.)

Neural circuitry underlying rule use in humans and nonhuman primates

J. Neurosci.

Neuropsychological and neuropathological sequelae of cerebral anoxia: a critical review

J. Int. Neuropsychol. Soc.

Review
A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes