Central to the concept of the “cognitive map” is that it confers behavioral flexibility, allowing animals to take efficient detours, exploit shortcuts, and avoid alluring, but unhelpful, paths. The neural underpinnings of such naturalistic and flexible behavior remain unclear. In two neuroimaging experiments, we tested human participants on their ability to navigate to a set of goal locations in a virtual desert island riven by lava, which occasionally spread to block selected paths (necessitating detours) or receded to open new paths (affording real shortcuts or false shortcuts to be avoided). Detours activated a network of frontal regions compared with shortcuts. Activity in the right dorsolateral PFC specifically increased when participants encountered tempting false shortcuts that led along suboptimal paths that needed to be differentiated from real shortcuts. We also report modulation in event-related fields and theta power in these situations, providing insight to the temporal evolution of response to encountering detours and shortcuts. These results help inform current models as to how the brain supports navigation and planning in dynamic environments.

Two fundamental questions underlie the expression of behavior, namely what to do and how vigorously to do it. The former is the topic of an overwhelming wealth of theoretical and empirical work particularly in the fields of reinforcement learning and decision-making, with various forms of affective prediction error playing key roles. Although vigor concerns motivation, and so is the subject of many empirical studies in diverse fields, it has suffered a dearth of computational models. Recently, Niv et al. [Niv, Y., Daw, N. D., Joel, D., & Dayan, P. Tonic dopamine: Opportunity costs and the control of response vigor. Psychopharmacology (Berlin), 191, 507–520, 2007] suggested that vigor should be controlled by the opportunity cost of time, which is itself determined by the average rate of reward. This coupling of reward rate and vigor can be shown to be optimal under the theory of average return reinforcement learning for a particular class of tasks but may also be a more general, perhaps hard-wired, characteristic of the architecture of control. We, therefore, tested the hypothesis that healthy human participants would adjust their RTs on the basis of the average rate of reward. We measured RTs in an odd-ball discrimination task for rewards whose magnitudes varied slowly but systematically. Linear regression on the subjects' individual RTs using the time varying average rate of reward as the regressor of interest, and including nuisance regressors such as the immediate reward in a round and in the preceding round, showed that a significant fraction of the variance in subjects' RTs could indeed be explained by the rate of experienced reward. This validates one of the key proposals associated with the model, illuminating an apparently mandatory form of coupling that may involve tonic levels of dopamine.

Perceptual decision-making performance depends on several cognitive and neural processes. Here, we fit Ratcliff's diffusion model to accuracy data and reaction-time distributions from one numerical and one verbal two-choice perceptual-decision task to deconstruct these performance measures into the rate of evidence accumulation (i.e., drift rate), response criterion setting (i.e., boundary separation), and peripheral aspects of performance (i.e., nondecision time). These theoretical processes are then related to individual differences in brain activation by means of multiple regression. The sample consisted of 24 younger and 15 older adults performing the task in fMRI before and after 100 daily 1-hr behavioral training sessions in a multitude of cognitive tasks. Results showed that individual differences in boundary separation were related to striatal activity, whereas differences in drift rate were related to activity in the inferior parietal lobe. These associations were not significantly modified by adult age or perceptual expertise. We conclude that the striatum is involved in regulating response thresholds, whereas the inferior parietal lobe might represent decision-making evidence related to letters and numbers.

Exploring a novel environment can facilitate subsequent hippocampal long-term potentiation in animals. We report a related behavioral enhancement in humans. In two separate experiments, recollection and free recall, both measures of hippocampus-dependent memory formation, were enhanced for words studied after a 5-min exposure to unrelated novel as opposed to familiar images depicting indoor and outdoor scenes. With functional magnetic resonance imaging, the enhancement was predicted by specific activity patterns observed during novelty exposure in parahippocampal and dorsal prefrontal cortices, regions which are known to be linked to attentional orienting to novel stimuli and perceptual processing of scenes. Novelty was also associated with activation of the substantia nigra/ventral tegmental area of the midbrain and the hippocampus, but these activations did not correlate with contextual memory enhancement. These findings indicate remarkable parallels between contextual memory enhancement in humans and existing evidence regarding contextually enhanced hippocampal plasticity in animals. They provide specific behavioral clues to enhancing hippocampus-dependent memory in humans.

How do visual luminance, shape, motion, and depth bind together in the brain to represent the coherent percept of a 3-D object within hundreds of milliseconds (msec)? We provide evidence from simultaneous magnetoencephalographic (MEG) and electroencephalographic (EEG) data that perception of 3-D objects defined by luminance or motion elicits sequential activity in human visual cortices within 500 msec. Following activation of the primary visual cortex around 100 msec, 3-D objects elicited sequential activity with only little overlap (dynamic 3-D shapes: MT-LO-Temp; stationary 3-D shapes: LO-Temp). A delay of 80 msec, both in MEG/EEG responses and in reaction times (RTs), was found when additional motion information was processed. We also found significant positive correlations between RT, and MEG and EEG responses in the right temporal location. After about 400 msec, long-lasting activity was observed in the parietal cortex and concurrently in previously activated regions. Novel time-frequency analyses indicate that the activity in the lateral occipital (LO) complex is associated with an increase of induced power in the gamma band, a hallmark of binding. The close correspondence of an induced gamma response with concurrent sources located in the LO in both experimental conditions at different points in time (∼200 msec for luminance and ∼300 msec for dynamic cues) strongly suggests that the LO is the key region for the assembly of object features. The assembly is fed forward to achieve coherent perception of a 3-D object within 500 msec.

We addressed the hypothesis that perceptual priming and explicit memory have distinct neural correlates at encoding. Event-related potentials (ERPs) were recorded while participants studied visually presented words at deep versus shallow levels of processing (LOPs). The ERPs were sorted by whether or not participants later used studied words as completions to three-letter word stems in an intentional memory test, and by whether or not they indicated that these completions were remembered from the study list. Study trials from which words were later used and not remembered (primed trials) and study trials from which words were later used and remembered (remembered trials) were compared to study trials from which words were later not used (forgotten trials), in order to measure the ERP difference associated with later memory (DM effect). Primed trials involved an early (200–450 msec) centroparietal negative-going DM effect. Remembered trials involved a late (900–1200 msec) right frontal, positive-going DM effect regardless of LOP, as well as an earlier (600–800 msec) central, positive-going DM effect during shallow study processing only. All three DM effects differed topographically, and, in terms of their onset or duration, from the extended (600–1200 msec) fronto-central, positive-going shift for deep compared with shallow study processing. The results provide the first clear evidence that perceptual priming and explicit memory have distinct neural correlates at encoding, consistent with Tulving and Schacter's (1990) distinction between brain systems concerned with perceptual representation versus semantic and episodic memory. They also shed additional light on encoding processes associated with later explicit memory, by suggesting that brain processes influenced by LOP set the stage for other, at least partially separable, brain processes that are more directly related to encoding success.