New perspectives on adolescent motivated behavior: attention and conditioning

Abstract

Adolescence is a critical transition period, during which fundamental changes prepare the adolescent for becoming an adult. Heuristic models of the neurobiology of adolescent behavior have emerged, promoting the central role of reward and motivation, coupled with cognitive immaturities. Here, we bring focus to two basic sets of processes, attention and conditioning, which are essential for adaptive behavior. Using the dual-attention model developed by Corbetta and Shulman (2002), which identifies a stimulus-driven and a goal-driven attention network, we propose a balance that favors stimulus-driven attention over goal-driven attention in youth. Regarding conditioning, we hypothesize that stronger associations tend to be made between environmental cues and appetitive stimuli, and weaker associations with aversive stimuli, in youth relative to adults. An attention system geared to prioritize stimulus-driven attention, together with more powerful associative learning with appetitive incentives, contribute to shape patterns of adolescent motivated behavior. This proposed bias in attention and conditioning function could facilitate the impulsive, novelty-seeking and risk-taking behavior that is typical of many adolescents.

Fig. 1

Articulation among attention, conditioning, and motivated behavior. This schematic describes how attention, conditioning and decision-making are tightly interdependent and significantly contribute to behavioral output. These operations can be organized along 3 sequential steps: (1) First, attention captures the context as a whole (e.g., visual scene of a crowd; hubbub). (2) It then selects a stimulus (e.g., the girl with a red sweater; song in the background). The critical notion here is that attention will select the most salient stimulus. Salience is determined either by the physical features of the stimulus (e.g., color red; favorite song), or by a preset goal or intention (e.g., looking for your friend who has a red coat). Schematically, the selective orienting by physical/perceptual characteristics is mediated by “stimulus-driven attention” mechanisms, whereas the selective orienting by internal rules/intentions is mediated by “goal-driven attention”. Stimuli can be endowed with affective value if they are systematically associated with other affectively-laden stimuli (e.g., song repeatedly heard during summer vacation becomes the favorite song). This is at this juncture that conditioning comes to play a critical role. A neutral stimulus conditioned to threat or to reward will acquire a unique salience that will determine the focus of selective attention. (3) Once attention orients selectively to an object, it maintains the focus on the object to permit, or prime, other cognitive processes to manipulate the information. These cognitive processes pertain mostly to executive function, e.g., working memory, inhibition, shift, plan, reversal, and they ultimately generate a course of action. The course of action is the behavioral output, which can be generalized as an approach or an avoidant response (Ernst et al., 2006). This latter hypothesis requires to be further qualified. The proposed valence bias in associative conditioning may be different for cue- and context-conditioning. Furthermore, the direction of the bias in cue-conditioning may depend on the context in which learning occurs. As a first iteration of this theory, we will make the case for a positive bias, with the understanding that this is only a first approximation awaiting systematic testing. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

Fig. 2

Model of the dual attention system (Corbetta and Shulman, 2002). (A) Information from an external stimulus can be processed along the following path. (1) Information from the retina about a stimulus (yellow sign) is first sent to the thalamus (through the LGN) (hatched black lines). (2) The thalamus dispatches the filtered information to cortex, as well as amygdala and striatum (these arrows are not shown here). (3) The occipital cortex carries this information to both the ventral (red lines) and dorsal attention (green lines) pathways. The ventral pathway will generate prepotent actions. The dorsal pathway will evaluate the information; activate rule representations that will engage networks to deal with the stimulus appropriately. The dorsal pathway can also influence prepotent responses through the modulation of the ventral pathway, here represented as the arrow from the DLPFC to the IFG/vPFC. (4) The amygdala and striatum receive, in addition to thalamic information, cortical information (arrows from thalamus to striatum and amygdala not represented here), and code the emotional/motivational value of the stimulus. This information is then shared with other brain areas, directly or through thalamic connections. Depending on the conditions of presentation of the stimuli (e.g., repeated pairing of stimuli), these subcortical structures may engage conditioning processes. DLPFC: dorsolateral prefrontal cortex; IFG: Inferior frontal gyrus; LGN: lateral geniculate nucleus; TPJ: temporoparietal junction; vPFC: ventral prefrontal cortex. (B) The upper panel schematizes the articulation between conditioning and attention in adolescents. The lower panel represents the simplified dual-attention system in adolescents. These functional patterns are likely to apply to specific conditions (e.g., in affectively charged contexts), which will need to be defined in future work. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)