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 response to stimuli, approach or avoidance (including no action, or withdrawal).
The Triadic Model provides a simple dynamic scheme of brain function that underlies motivated behavior (). It is based on the premises that responses to stimuli represent the output of the functional integration of three distinct, although overlapping, systems. One system exerts a preferential role in approach behavior and relies on striatal circuits. The second system has a dominant role in avoidance behavior and relies on amygdala circuits. The third system exerts a regulatory control over both approach and avoidance responses and relies on the medial prefrontal cortex. Although these systems are heterogeneous with respect to both anatomy and function (), ample evidence indicates a dominant role for each of them along the lines proposed by the Triadic Model (see review, Ernst et al. 2006
Figure 1 Triadic Model. This model is a heuristic representation of a neural systems approach to the neurobiology of motivated behavior. Generically, behavior results from the integration of signals underlying the coding of approach, the coding of avoidance and (more ...)
Anatomical and functional heterogeneity of the triadic nodes
This scheme integrates four sources of data, (1) behavioral deficits observed in human lesion studies (e.g., Bechara and Van Der, 2005
; Fellows and Farah, 2005
; Seitz et al., 2006
); (2) findings from functional neuroimaging of the developing brain (Ernst and Hardin, 2008
), (3) cognitive neuroscience theories of motivated behavior (functional specialization of brain systems) (see review, Ernst and Paulus, 2005
), and (4) a dual-system theory of behavior applied to temperament and personality research (Gray, 1972
; Pickering and Gray, 2001
First, lesion studies in humans provide invaluable information on the role of brain regions in behavior. They are particularly useful for identifying “essential” or “dominant” functions of these structures. However, a number of caveats limit the generalizability of the findings. Among them is the difficulty of assessing accurately the anatomical boundaries of the lesions. As a consequence, the over- or under-inclusion of anatomical regions involved in these lesions can provide inaccurate links between brain structures and clinical pictures. Another caveat is the absence of pre-lesion neuropsychological assessment limits the ability to definitively attribute deficits to the lesions. This issue is often compounded by limited sample sizes. Finally, the nature of the pathology leading to the brain lesions may itself be responsible for some aspects of the behavioral deficits.
With regard to the triadic nodes, certain pathologies affecting the amygdala are very specific (e.g., Urbache-Weithe disease) and provide important information on the function of this structure (see below). In contrast, lesions of the striatum are usually large, often secondary to anoxic events (Caine and Watson, 2000
), and may not be quite specific to the function of these structures. Similarly, prefrontal cortical lesions are variable and specific regions are more difficult to assess with precision, although meta-analyses of lesion studies are beginning to provide reliable findings (e.g., Seitz et al., 2006
). The most consistent reports suggest that amygdala lesions are associated with deficits in response to negative stimuli (Adolphs et al., 1994
; Berntson et al., 2007
) and striatal regions are associated with amotivation and reduction of motor initiation (e.g., Adam et al., 2008
). Prefrontal cortical regions highly depend highly on the regions being affected. The ventromedial PFC has been consistently associated with deficits in inhibition and decision-making (see review, Bechara and Van Der, 2005
). In contrast, the medial prefrontal cortex has been found to contribute to self-reflection, regarding action more dorsally, and emotion more ventrally (Seitz et al. 2006
). These findings of human lesion studies seem to support the general lines of the Triadic Model.
Second, neuroimaging findings suggest functional differences between adolescents and adults in response to reward-related stimuli. Some of these studies reflect enhanced responsivity of the striatal system to appetitive stimuli, reduced involvement of the amygdala in response to negative stimuli, and reduced contribution of prefrontal cortex in choice selection in adolescents compared to adults, although these findings are not all consistent (Ernst and Hardin, 2008
Third, cognitive neuroscience has provided a systematic approach to the study of complex processes such as decision-making or motivated behaviors, based on the decomposition of these processes into smaller elements more amenable to scientific scrutiny. This approach is typically used to develop paradigms and to provide a strategy for the neuroimaging analyses of these paradigms.
Fourth, the dual-system theory is based on a reduction of behavior patterns into two separate response modes, approach, and avoidance, that are subserved by two separate neurobehavioral systems (Gray, 1972
). This framework is used extensively in research on temperament and personality (Pickering and Gray, 2001
). In general, the neuroimaging literature in adults tend to support the notion of separate, yet overlapping, systems coding for approach and avoidance. In addition, an overall supervisory system (the prefrontal cortex) has been described as a regulator of behavior.
Neuroimaging studies in adults consistently report recruitment of striatal regions during reward-related processes (Breiter et al., 2001
; Delgado et al., 2000
; Ernst et al., 2005
; Knutson et al., 2001
; Knutson et al., 2003
; O’Doherty et al., 2004
; Rogers et al., 2004
). Conversely, amygdala, hippocampus, and insula are most commonly recruited in response to unfavorable or aversive outcomes (Becerra et al., 2001
; LeDoux, 2000
; Tom et al., 2007
; Zald and Pardo, 1997
). Recruitment of the striatum in conjunction with negative outcomes (Becerra et al. 2001
; Jensen et al., 2003
; Seymour et al., 2007
), and amygdala in conjunction with positive outcome is also reported, however less frequently (Becerra et al. 2001
; Jensen et al. 2003
; Seymour et al. 2007
; Zalla et al., 2000
). Medial prefrontal structures are recognized for their role in modulating affective and cognitive processes.
Regional functional specialization is also emerging from the extant literature. For example, orbital and medial prefrontal regions have been implicated in the representations of affective values (O’Doherty et al., 2003
; O’Doherty, 2007
; Rolls, 2004
), inhibition (Elliott and Deakin, 2005
; Yucel et al., 2007
), response reversal (Schoenbaum et al., 2007
), and conflict resolution (Yeung et al., 2004
). The anterior medial PFC has been associated with metacognition (Fletcher et al., 1995
; Gallagher et al., 2000
), self-evaluation (Amodio and Frith, 2006
; Kelley et al., 2002
; O’Doherty et al. 2003
) and rule formation (Bunge et al., 2005
). These high-level cognitive functions integrate information about endogenous (physical and emotional state) and exogenous environment to modulate behavioral output. Some of this information is provided by loops through the amygdala and striatum.
The main point of this discussion is three-fold: (1) the processing of outcome is occurring throughout the triadic system, engaging amygdala, striatum, and prefrontal cortex. (2) However, each node is engaged distinctly, and the relative contribution of these regions depends on a number of factors, one of them being outcome valence, i.e., how attractive or aversive the outcome is. Other factors include experimental conditions, such as the stage of decision-making under study (selection, vs. anticipation, vs. outcome), the modulation of probability or timing of outcomes, or the use of contingencies to the delivery of rewards, such as performing well on a cognitive task. Because of the influence of experimental conditions on regional activation, discrepant results among studies can clearly be an effect of the different paradigms being used. (3) Finally, the most consistent finding across studies is a bias of the amygdala (and associated circuitry) to be recruited in the presence of negative stimuli, and of the striatum (and associated circuitry) to be recruited in the presence of positive stimuli. This valence-related bias emerges against a role of these structures in the coding of both positive and negative affective polarities.
These three nodes of behavioral control, centered on the striatum, amygdala, and prefrontal cortex, constitute the backbone of the Triadic Model. The functional connections among these three centers and their development are beginning to be mapped out, as discussed in the following section.