Animal research suggests that neural systems are fundamentally organized to discriminate conditions of low resources and unmet energy needs from conditions of high resources and met energy needs and to regulate behavior, effort, autonomic function, and homeostasis accordingly (Schneider et al. Reference Schneider, Wise, Benton, Brozek and Keen-Rhinehart2013). Energy acquisition and storage are an important prerequisite for reproductive success. Thus, in most species, behavioral sequences are organized so that a period of eating and fattening often precedes mating and caring for offspring. This is particularly important in habitats where food availability fluctuates or is unpredictable (Schneider et al. Reference Schneider, Wise, Benton, Brozek and Keen-Rhinehart2013). Perceptions of having a surplus of resources and energy shift the regulatory focus from immediate, momentary concerns and harm prevention toward future-directed behavior and investments.

Based on this fundamental organization of neural systems, we recently proposed a neurobehavioral theory of predictive and reactive control systems (PARCS; Tops et al. Reference Tops, Boksem, Quirin, IJzerman and Koole2014; Reference Tops, Quirin, Boksem and Koole2017). PARCS integrates evidence of separate neural systems that control behavior, autonomic responses, and homeostasis in predictable, familiar, and stable environments versus unpredictable, unstable, and novel environments, respectively. PARCS suggests that a ventral, reactive control system evolved for the purpose of processing novelty and biological salience to control behavior in unpredictable as well as urgent and emergency situations. It responds in a feedback-guided manner to the immediate situation and focuses attention narrowly on the local situation. This system includes areas such as the anterior insula (AI), inferior frontal gyrus (IFG), amygdala, and ventral striatum. On the other hand, PARCS suggests that the dorsal, predictive control system engages in creating internal models that predict future outcomes through simulation and updates those models slowly during learning, in line with the idea that it responds to environmental predictability and familiarity. This system implements feed-forward action control and includes areas such as the posterior cingulate cortex, precuneus, dorsolateral prefrontal cortex, and dorsal striatum.

Learning of a novel task involves a ventral-to-dorsal shift in reactive-to-predictive (and eventually habitual) processing through corticostriatal neural loops, forming schemata and predictive internal models for efficient task performance (Tops & Boksem Reference Tops and Boksem2012; cf. Alcaro & Panksepp Reference Alcaro and Panksepp2011). Based on the physiology and behavioral pharmacology of different parts of the striatum, it has been proposed that the ventral striatum responds to temporally unpredictable stimuli (which require interruption of ongoing behavior) and that the dorsal striatum responds to temporally predictable stimuli (i.e., stimuli that are so predictable that animals engage in behavior just prior to the stimulus; Nicola Reference Nicola2007). Similar to temporally unpredictable stimuli, reward uncertainty may activate the ventral striatum and require reactive control, because uncertainty of reward delivery produces prediction error signals that interrupt routinized responding.

Based on the above, we suggest that “incentive hope” reflects a type of anticipation that involves the activation of reactive control in unpredictable circumstances. This anticipation involves focused attention on the here and now. At first sight, this focus on the here and now sounds contradictory to “anticipatory.” But it is central to reactive control: If the onset of an appetitive or aversive stimulus is unpredictable but potentially impending, then reactive control (i.e., focus on the here and now) is kept in ready mode (sustained attention, vigilance) for immediate feedback-guided responses to the stimulus. The resulting prolonged sense of immediacy is characteristic of anticipatory anxiety, which makes this anxiety condition aversive with intense responses to pain and other aversive stimuli. The prolonged sense of immediacy likewise invigorates responding to appetitive stimuli: The prolonged focused processing of a potentially impending food stimulus magnifies the motivational processes underpinning food seeking under uncertainty. Although this mode of response/appraisal readiness does not involve prospection based on predictive control and internal models, it is anticipatory because reactive control (in response to unpredictability and conditioned stimuli) puts goal, task, and target stimulus activations in a maintenance working memory buffer. Such functions of reactive system areas such as the IFG are well reported in the neuroimaging literature (e.g., Blumenfeld & Ranganath Reference Blumenfeld and Ranganath2007; De Baene et al. Reference De Baene, Albers and Brass2012; Hampshire et al. Reference Hampshire, Thompson, Duncan and Owen2009; Owen et al. Reference Owen, Herrod, Menon, Clark, Downey, Carpenter, Minhas, Turkheimer, Williams, Robbins, Sahakian, Petrides and Pickard1999). For instance, the IFG may project back to the temporal lobe to keep representations active, allowing for stimuli and task set to interact when coming in sequentially (e.g., Assadollahi & Rockstroh Reference Assadollahi and Rockstroh2008).

The state of readiness in anticipation of unpredictably timed or uncertain stimuli is also required in vigilance tasks that activate a set of mainly right-lateralized brain regions that may form the core network subserving vigilant attention in humans, including IFG, AI, and the temporoparietal junction (Langner & Eickhoff Reference Langner and Eickhoff2013). Moreover, often right-lateralized reactive system areas in the IFG and AI have been implicated in incentive motivation (Naqvi & Bechara Reference Naqvi and Bechara2009), anticipation of pleasant and aversive stimuli (Knutson & Greer Reference Knutson and Greer2008), and anticipatory anxiety (Carlson et al. Reference Carlson, Greenberg, Rubin and Mujica-Parodi2011; Simmons et al. Reference Simmons, Stein, Strigo, Arce, Hitchcock and Paulus2011). For instance, suggesting that the AI is preparing for the sensory and affective impact of the stimulus, the degree of activation in the AI during anticipation is correlated with experienced stimulus intensity and with the degree of activation in the caudate during stimulus processing (Lovero et al. Reference Lovero, Simmons, Aron and Paulus2009). Additionally, the AI shows sustained activation by unpredictable but not predictable threat (Alvarez et al. Reference Alvarez, Chen, Bodurka, Kaplan and Grillon2011).

Anticipatory processing in reactive control may be implicated in the potentiation of incentive motivation under conditions of reward uncertainty (hope) and punishment uncertainty (apprehension), both for uncertain delivery and timing. In obese subjects, AI revealed increased functional and effective connectivity in response to food cues, especially to striatal regions (Garcia-Garcia et al. Reference Garcia-Garcia, Jurado, Garolera, Segura, Sala-Llonch, Marques-Iturria, Pueyo, Sender-Palacios, Vernet-Vernet, Narberhaus, Ariza and Junqué2012; Kullmann et al. Reference Kullmann, Pape, Heni, Ketterer, Schick, Haring, Fritsche, Preissl and Veit2013; Nummenmaa et al. Reference Nummenmaa, Hirvonen, Hannukainen, Immonen, Lindroos, Salminen and Nuutila2012). In posttraumatic stress disorder, a disorder associated with the experience of decreased predictability and control, excessive anticipatory reaction of the AI to temporally unpredictable aversive stimuli related to greater perceived threat (Simmons et al. Reference Simmons, Norman, Spadoni and Strigo2013). These examples illustrate that, through the overlap of incentive hope and apprehension in reactive control, PARCS theory may explain why anxious individuals show stronger potentiation of incentive motivation under conditions of reward uncertainty (Hellberg et al. Reference Hellberg, Levit and Robinson2018).