Because little is known about the human trait of affiliation, we provide a novel neurobehavioral model of affiliative bonding. Discussion is organized around processes of reward and memory formation that occur during approach and consummatory phases of affiliation. Appetitive and consummatory reward processes are mediated independently by the activity of the ventral tegmental area (VTA) dopamine (DA)–nucleus accumbens shell (NAS) pathway and the central corticolimbic projections of the u-opiate system of the medial basal arcuate nucleus, respectively, although these two projection (...) systems functionally interact across time. We next explicate the manner in which DA and glutamate interact in both the VTA and NAS to form incentive-encoded contextual memory ensembles that are predictive of reward derived from affiliative objects. Affiliative stimuli, in particular, are incorporated within contextual ensembles predictive of affiliative reward via: (a) the binding of affiliative stimuli in the rostral circuit of the medial extended amygdala and subsequent transmission to the NAS shell; (b) affiliative stimulus-induced opiate potentiation of DA processes in the VTA and NAS; and (c) permissive or facilitatory effects of gonadal steroids, oxytocin (in interaction with DA), and vasopressin on (i) sensory, perceptual, and attentional processing of affiliative stimuli and (ii) formation of social memories. Among these various processes, we propose that the capacity to experience affiliative reward via opiate functioning has a disproportionate weight in determining individual differences in affiliation. We delineate sources of these individual differences, and provide the first human data that support an association between opiate functioning and variation in trait affiliation. Key Words: affiliation corticolimbic-striatal networks; appetitive and consummatory reward; dopamine; oxytocin; personality; social bonds; social memory; u-opiates. (shrink)

Commentary on our target article centers around six main topics: (1) strategies in modeling the neurobehavioral foundation of human behavioral traits; (2) clarification of the construct of affiliation; (3) developmental aspects of affiliative bonding; (4) modeling disorders of affiliative reward; (5) serotonin and affiliative behavior; and (6) neural considerations. After an initial important research update in section R1, our Response is organized around these topics in the following six sections, R2 to R7.

Depue & Morrone-Strupinsky's (D&M-S's) language suggests that, unlike Kent Berridge, they may allow that the activity of a largely subcortical system, which is presumably often introspectively and cognitively inaccessible, constitutes affectively felt experience even when so. Such experience would then be phenomenally conscious without being reflexively conscious or cognitively access-conscious, to use distinctions formulated by the philosopher Ned Block.

Depue & Morrone-Strupinsky (D&M-S) do not address how a reward system accommodates the motivational dilemmas associated with (a) the decision to approach versus avoid conspecifics, and (b) self versus other tradeoffs inherent in behaving altruistically toward bonded relationship partners. We provide an alternative evolutionary view that addresses motivational conflict, and discuss implications for the neurobiological study of affiliative bonds.

Depue & Morrone-Strupinsky's (D&M-S's) implicit assumption appears to be that affiliative bonding is either strengthened or maintained with time; however, it is more realistic that it can also be weakened or destroyed by conflictive interpersonal interactions. Without specifying the mechanisms by which antagonistic stimuli deteriorate affiliative bonding, the model is incapable of accounting for the dynamics associated with this complex phenomenon.

Depue & Morrone-Strupinsky (D&M-S) present a thorough case for the role of “reward” brain circuits in affiliative bonding. Integration of information in the nucleus accumbens shell (NA), the role of dopamine in this processing, and opioid (primarily via mu receptors) control of these circuits are the primary elements of the model. Although the overall picture is quite compelling, the description leans excessively in the view of dopamine systems as “reward” circuits.

Depue & Morrone-Strupinsky's (D&M-S's) model of affiliation meets the criteria advanced for the definition of behavior systems and endophenotypes. We argue that its application in psychiatry could be useful for identifying a biological pathophysiology common to a variety of conditions that are currently classified in very different categories of psychiatric nosography, including autism, schizoid personality, primary psychopathy, and dismissing attachment.

Depue & Morrone-Strupinsky (D&M-S) have elaborated a detailed description of the motivational system for affiliation and its neurological basis. This “bottom-up” approach, based almost entirely on studies of nonhuman species, fails to connect with personality differences at the human level. A “top-down” approach looks for common biological markers in human and nonhuman species and relates these to behavior in both.

This commentary speaks to the relationship between Depue & Marrone-Strupinsky's (D&M-S's) concept of trait affiliation and affiliative memory and the formation of human community, especially among peer groups. The target article suggests a model for how and why dynamic communities form in a number of disparate contexts and under a number of circumstances.

Miller and Rodgers (2001) proposed a central nervous system based Ontogenetic Bonding System that operates across the life course to promote succorant, 1 affiliative, sexual, and nurturant bonds. I discuss features of this theoretical framework that can inform Depue & Morrone-Strupinsky's (D&M-S's) model. Most important, I suggest that the affiliative reward processes D&M-S describe are better conceptualized as subserving the affect/motivation of affection. Footnotes1 “Succorance” is a term coined by Murray (1938) to describe a general tendency to seek the (...) help and protection of others. (shrink)

The construct for affiliation in Depue & Morrone-Strupinsky's (D&M-S's) study is restricted to the interpersonal domain. This restriction is not found in other disciplines. It may be necessary in early stages of trait research. But the construct will need to be expanded to speak to the more complex, second-order affiliations of which humans are capable.

The possible role of the neurotransmitter serotonin in human affiliative behavior is under-examined in the review by Depue & Morrone-Strupinsky (D&M-S). This commentary reviews evidence indicating that serotonin not only inhibits aggressive behavior that may be detrimental to affiliative bonds with others in a social group but serotonin also enhances prosocial behaviors that may facilitate ties to the social group.