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.

in addition to endogenously produced opiates, which are part of normal affiliative neurocircuitry and attachment formation, exogenous opiates – such as drugs of addiction and abuse – may affect affiliation. we consider possible modulatory effects of such exogenous opiates on the development of early parent–infant attachment from both parents' and infants' perspectives.

brain opioids regulate social emotions in several distinct ways. the abundance of neuroscientific detail in the target article helps familiarize the uninitiated with the true and humbling complexities of mammalian brains, but little of it translates to research strategies, with robust predictions, at the human level. only global neurochemical affective state variables derived from animal research have clear implications for human research.

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.

the dynamic developmental theory of attention-deficit/hyperactivity disorder (adhd) proposes that hypodopaminergic functioning results in anomalous delay-of-reinforcement gradients in adhd, which in turn might account for many of the observed behavioral and cognitive characteristics. however, hyperdopaminergic functioning might also impair mnemonic representation of codes for spatial, motoric, and reward information and contribute to the purported shorter delay gradients in adhd.

In the present commentary we expand on two concepts relevant to understanding affliliative bonding. Differences and similarities between the functions and actions of oxytocin and vasopressin are difficult to study but may be critical to an understanding of mechanisms for social bonding. What is termed here a “trait of affiliation” may reflect in part the capacity of these same peptides to program the developing nervous system.

affect mirroring allows infants to distinguish emotional and intentional states of significant others, which – in the pursuit of their own drive satisfaction, including satisfaction of the affiliative drive – become important contextual stimuli predictive of reward. learning to perceive and manipulate others' attitudes toward oneself in pursuit of affiliative reward may be an important step in social development that is impaired in autism.

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’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.

notwithstanding the many strengths of the dynamic developmental theory, there remain challenges to be overcome before it can be incorporated into a true causal model of attention-deficit/hyperactivity disorder (adhd). these include the development of reliable measures of reinforcement delay gradients, the validation of shortened reinforcement delay as an endophenotype, and the integration of this pathway with other potential pathways.

despite general agreement that altered reward sensitivity is involved in attention-deficit/hyperactivity disorder (adhd), a wide range of different alterations has been proposed. we cite work showing abnormal sensitivity to delay of reward, together with abnormal sensitivity to individual instances of reward. we argue that at the cellular level these behavioural characteristics might indicate that dopamine timing is off in children with adhd.

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.

Miller and Rodgers (2001) proposed a central nervous system based Ontogenetic Bonding System that operates across the life course to promote succorant, 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.

Support for a neurobiological distinction between affiliation (Attachment) and agency (Achievement) was achieved by comparing responses to a dopaminergic (DA) and a serotonergic (5-HT) challenge test. DA responses were similar, but a 5-HT modulation of DA emerged for Achievement and not for Attachment. Molecular genetics performed on Panksepp’s dimension “Care” revealed an association with a polymorphism of the DA catabolizing enzyme COMT that was not associated with separation distress.

primate research suggests that affiliation is a highly complex construct. studies of primate affiliation demonstrate the need to distinguish between various affiliative behaviors, consider relationships as emergent properties of these behaviors, define affiliation in the context of general environmental responsiveness, and address developmental changes in affiliation across the lifespan.

Research on the neurobiology and psychosocial features of Major Depressive Disorder has the ability to extend our understanding of affiliative behavior. In depression, decreased hedonic capacity and hypoactivity in dopaminergic and prefrontal circuitries may decrease the ability to experience affiliative relationships as rewarding. We suggest that neurobiological research on depression can provide a test case for theoretical models of affiliation.

sagvolden, johansen, aase, and russell (sagvolden et al.) examine attention-deficit/hyperactivity disorder (adhd) at levels of analysis ranging from neurotransmitters to behavior. at the behavioral level they attribute aspects of adhd to anomalies of delay-of-reinforcement gradients. with a normal gradient, responses followed after a long delay by a reinforcer may share in the effects of that reinforcer; with a diminished or steepened gradient they may fail to do so. steepened gradients differentially select rapidly emitted responses (hyperactivity), and they limit the effectiveness with which extended stimuli become conditioned reinforcers, so that observing behavior is less well maintained (attention deficit). impulsiveness also follows from steepened gradients, which increase the effectiveness of smaller, more immediate consequences relative to larger, more delayed ones. individuals who vary in the degree to which their delay gradients are steepened will show different balances between hyperactivity and attention deficit. given the range of adhd phenomena addressed, it may be unnecessary to appeal to additional behavioral processes such as extinction deficit. extinction deficit is more likely a derivative of attention deficit, in that failure to attend to stimuli differentially correlated with extinction should slow its progress. the account suggests how relatively small differences in delay gradients early in development might engender behavioral interactions leading to very large differences later on. the steepened gradients presumably originate in properties of neurotransmitter function, but behavioral interventions that use consistently short delays of reinforcement to build higher-order behavioral units as a scaffolding to support complex cognitive and social skills may nonetheless be feasible.

the reinforcement/extinction disorder hypothesis (sagvolden et al.) is an important counterweight to the executive dysfunction model of attention-deficit/hyperactivity disorder (adhd). however, like that model, it conceptualises adhd as pathophysiologically homogeneous, resulting from a common core dysfunction. recent studies reporting neuropsychological heterogeneity suggest that this common core dysfunction may be the scientific equivalent of a red herring.

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.

the authors regard opiates as the primary neural substrate for social attachment, and peptide hormones as subsidiary. one may instead conclude from their evidence that oxytocin, vasopressin, and opiates play complementary roles in attachment. oxytocin and vasopressin relate to different aspects of emotional experience, and opiates to quiescence from long-term attachment. this is related to intimacy versus affiliation.