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.

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.

previous research into human traits has reached impressive consensus regarding at least some traits, but recent evidence suggests these to be genetically heterogeneous. this is problematic for theories of the neurobiology of human traits. future research should more closely integrate genetic, behavioral, and psychometric research to arrive at biologically validated measurement instruments, which may be better used to understand the mediating role of these traits in the association between genetic variants and complex behaviors.

in this commentary, i argue that the theory presented by sagvolden et al. can be much stronger if its scope is limited, if its developmental aspects are refined, if it can be made to generate testable predictions, and if it can be supported with more data from humans.

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.

Attention-deficit/hyperactivity disorder (ADHD) is currently defined as a cognitive/behavioral developmental disorder where all clinical criteria are behavioral. Inattentiveness, overactivity, and impulsiveness are presently regarded as the main clinical symptoms. The dynamic developmental behavioral theory is based on the hypothesis that altered dopaminergic function plays a pivotal role by failing to modulate nondopaminergic (primarily glutamate and GABA) signal transmission appropriately. A hypofunctioning mesolimbic dopamine branch produces altered reinforcement of behavior and deficient extinction of previously reinforced behavior. This gives rise to delay aversion, development of hyperactivity in novel situations, impulsiveness, deficient sustained attention, increased behavioral variability, and failure to “inhibit” responses (“disinhibition”).

A hypofunctioning mesocortical dopamine branch will cause attention response deficiencies (deficient orienting responses, impaired saccadic eye movements, and poorer attention responses toward a target) and poor behavioral planning (poor executive functions). A hypofunctioning nigrostriatal dopamine branch will cause impaired modulation of motor functions and deficient nondeclarative habit learning and memory. These impairments will give rise to apparent developmental delay, clumsiness, neurological “soft signs,” and a “failure to inhibit” responses when quick reactions are required.

A hypofunctioning mesocortical dopamine branch will cause attention response deficiencies (deficient orienting responses, impaired saccadic eye movements, and poorer attention responses toward a target) and poor behavioral planning (poor executive functions). A hypofunctioning nigrostriatal dopamine branch will cause impaired modulation of motor functions and deficient nondeclarative habit learning and memory. These impairments will give rise to apparent developmental delay, clumsiness, neurological “soft signs,” and a “failure to inhibit” responses when quick reactions are required.

whether or not trait affiliation correlates with human behaviour needs investigating. one should be careful generalizing neuropsychological mechanisms for affiliation, and generalizing an analysis based on one or two neuropsychological mechanisms and mostly studies on rodents, to complex human social interactions. serotonin is an example of a neurotransmitter playing an important role in cooperation and interacting with the dopaminergic system.

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.

Early and automatic neuropsychological processes may be influenced by altered dopaminergic functions but cannot be fully explained by these or by altered reinforcement and extinction processes. The reinforcement- extinction model is excellent for understanding certain causal pathways of attention-deficit/hyperactivity disorder (ADHD), but it can hardly explain the heterogeneous developmental trajectories of ADHD fully. It should be integrated into a multiple pathways model.

In the target article, Sagvolden and collaborators propose that attentional-deficit/hyperactivity disorder (ADHD) is the result of a general behavioral deficit which is mainly caused by a hypofunctioning mesolimbic dopaminergic system. Although we partly agree with this view, we think that it tends to overlook the dysfunction of prefrontal and frontostriatal executive functions by considering them to be a consequence of alterations in reward and extinction mechanisms. Rather, we believe that ADHD is the result of an overall cognitive and behavioral condition, associated to a generalized dopaminergic network dysfunction, and may not be easily attributable to a single basic behavioral function.

the “dynamic developmental” theory of attention-deficit/hyperactivity disorder (adhd) has come full circle from wender's (1971) reinforcement hypothesis. by specifying the principle of time constraints on reinforcement and extinction, the present theory allows for empirical validation. however, the theory implies, but does not discuss, implications for the neurophysiology of comorbidity in adhd. the authors' attribution of comorbid oppositional behavior to parental and societal reinforcement leaves out biological factors.

correcting the relationship between tonic and burst firing modes in dopamine neurons may help normalise stimulus-reinforcement gradients and contingent behaviour in attention-deficit/hyperactivity disorder (adhd) children. but appropriate evaluations of stimuli for developing adaptive plans and controlling impulsivity will not occur without moderating the gain-like functions of serotonin. the “dynamic theory” correctly highlights the need to account for variability in adhd. the dysmaturation of pre-executive information processing is proposed as an explanation.

at the core of the article by sagvolden and colleagues there is a set of data that throws light on an aspect of the adhd phenomenon. but one asks if the authors are a measure too brave to generalise so broadly from the unusually steep reinforcement gradients reported for the human condition and an animal model to the syndrome as a whole.

attention-deficit/hyperactivity disorder (adhd) represents adaptation to defective neurotransmission – an adaptation seldom with benefit. the resulting behavioural style not only increases vulnerability to adverse experiences, but also creates a context in which encountering adversity is more likely. furthermore, the fact that adhd is a highly heritable condition increases the probability of a child with a compromised neurobiological disposition being raised by caregivers with suboptimal resources.

Both the target article and the precommentary demonstrate that relatively simple biobehavioral processes have the cumulative effect of fostering behavioral outcomes characteristic of attention-deficit/hyperactivity disorder (ADHD). As such, the articles illustrate a central theme of Darwinian thinking – basic processes acting over time can produce complex and diverse outcomes. In this commentary, we indicate that tracing the action of processes over time can be facilitated by quantitative methods such as artificial neural networks.

sleep disturbances are common for children with attention-deficit/hyperactivity disorder (adhd) and are of great clinical significance. brain dopamine plays an important role for both adhd symptoms and sleep-wake regulation. we therefore suggest that one basic aspect of integrative brain-behavior relationship such as the sleep-wake cycle may certainly be addressed in a dynamic developmental theory of adhd.

trust is a temporary attachment between humans that pervades our daily lives. recent research has shown that the affiliative hormone oxytocin rises with a social signal of interpersonal trust and is associated with trustworthy behavior (the reciprocation of trust). this commentary reports these results and relates them to the target article's findings for variations in affiliative-related behaviors.

In Sagvolden et al.’s conceptualization of how a poor behavioral, social, and academic repertoire arises from an impaired interaction with the environment of an individual with a neurological disorder, we see a convergence between the medical diagnosis and the functional assessment on which the behavioral educational approach is based. If children with such a disorder do show delay-of-reinforcement steepened gradients, it is possible to predict their behavior under given circumstances. This could bring us to more precise diagnostic criteria and better intervention techniques.

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.

we have shown in a computational model that a poor memory for context could result in some of the behaviors associated with adhd, which is well in line with the dynamic developmental theory. given the important role of context in extinction, a weaker context due to a steeper delay-of-reinforcement gradient would result in impaired inhibition.

The “dynamic developmental theory” is based on hypofunctioning dopamine systems that follow an early overactivity phase. The theory does not consider recent experimental evidences from different attentiondeficit/ hyperactivity disorder (ADHD) models and the heterogeneity of the disorder. Alternatives are proposed that integrate available information gathered from clinical and experimental studies, with theoretical constructs.