Childhood exercise predicts response inhibition in later life via changes in brain connectivity and structure.

Participation in exercise during early life (i.e., childhood through adolescence) enhances response inhibition; however, it is unclear whether participation in exercise during early life positively predicts response inhibition in later life. This historical cohort study was designed to clarify whether participation in exercise (e.g., structured sports participation) during early life predicts response inhibition in adulthood and if so, to reveal the brain connectivity and cortical structures contributing to this association. We analyzed data derived from 214 participants (women = 104, men = 110; age: 26‒69 years). Results indicated that participation in exercise during childhood (before entering junior high school; ≤ 12 years old) significantly predicted better response inhibition. No such association was found if exercise participation took place in early adolescence or later (junior high school or high school; ≥ 12 years old). The positive association of exercise participation during childhood with response inhibition was moderated by decreased structural and functional connectivity in the frontoparietal (FPN), cingulo-opercular (CON), and default mode networks (DMN), and increased inter-hemispheric structural networks. Greater cortical thickness and lower levels of dendritic arborization and density in the FPN, CON, and DMN also moderated this positive association. Our results suggest that participation in exercise during childhood positively predicts response inhibition later in life and that this association can be moderated by changes in neuronal circuitry, such as increased cortical thickness and efficiency, and strengthened inter-hemispheric connectivity.

Urgency Promotes Affective Disengagement: Effects From Bivalent Cues on Preference Formation for Abstract Images.

Although previous research has characterized the important role for spatial and affective pre-cues in the control of visual attention, less is known about the impact of pre-cues on preference formation. In preference formation, the gaze cascade phenomenon suggests that the gaze serves both to enhance and express "liking" during value-based decision-making. This phenomenon has been interpreted as a type of Pavlovian approach toward preferred objects. Decision-making here reflects a process of gradual commitment in which the gaze functions as a precursor to choice; by this account, overt attention produces a necessarily positive, additive effect on the value of the attended object. The implication is that drawing attention to an object should initiate, and therefore promote, preference formation for that object. Alternatively, information-integration models of attention propose that attention produces a multiplicative effect on the value of the attended object, implying that negative information can impede preference formation. To pitch the gradual-commitment hypothesis against the information-integration hypothesis, we conducted four experiments that combined the spatial-cueing paradigm with a value-based choice paradigm. In each trial in all experiments, subjects were presented with an irrelevant, peripheral pre-cue for a duration of 500 ms, followed by a 500 ms blank, and then a pair of abstract images (one at the pre-cued position; one in the opposite hemifield). The subjects were asked to choose their preferred abstract image by pressing the corresponding button. We manipulated the type of pre-cues (images of faces versus foods; with varying affective associations) and the time constraints (a deadline of 1,500 ms versus self-paced). Overall, the choice data showed a clear pattern of influence from the pre-cues, such that, given a deadline, abstract images were chosen less often if they had been preceded by a pre-cue with a negative affective association (both for face and food images). Analyses of the gaze data showed the emergence of significant gaze biases in line with the subjects' choices. Taken together, the data pattern provided support for the information-integration hypothesis, particularly under urgency. When tasked with a speeded preference choice, subjects showed affective disengagement following pre-cues that carried a negative association.

Evaluative Processing of Food Images: Longer Viewing for Indecisive Preference Formation.

The well-known gaze cascade hypothesis proposes that as people look longer at an item, they tend to show an increased preference for it. However, using single food images as stimuli, we recently obtained results that clearly deviated from the general proposal that the gaze both expresses and influences preference formation. Instead, the pattern of data depended on the self-determination of exposure duration as well as the type of evaluation task. In order to disambiguate how the type of evaluation determines the relationship between viewing and liking we conducted the present follow-up study, with a fixed response set size as opposed to the varying set sizes in our previous study. In non-exclusive evaluation tasks, subjects were asked how much they liked individual food images. The recorded response was a number from 1 to 3. In exclusive evaluation tasks, subjects were asked for each individual food image to give one of three response options toward a limited selection: include it, exclude it, or defer the judgment. When subjects were able to determine the exposure duration, both the non-exclusive and exclusive evaluations produced inverted U-shaped trends such that the polar ends of the evaluation (the positive and negative extremes) were associated with relatively short viewing times, whereas the middle category had the longest viewing times. Thus, the data once again provided firm evidence against the notion that longer viewing facilitates preference formation. Moreover, the fact that non-exclusive and exclusive evaluation produced similar inverted U-shaped patterns suggests that the response set size is the critical factor that accounts for the observations here versus in our previous study. When keeping the response set size constant, with an equal opportunity to observe inverted U-shaped patterns, the findings are suggestive of a role for the level of decisiveness in determining the length of viewing time. For items that can be categorically identified as positive or negative, the evaluations are soon completed, with relatively brief viewing times. The prolonged visual inspection for the middle category may reflect doubt or uncertainty during the evaluative processing, possibly with an increased effort of information integration before reaching a conclusion.

Active Confirmation Bias in the Evaluative Processing of Food Images.

Predictive processing is fundamental to many aspects of the human mind, including perception and decision-making. It remains to be elucidated, however, in which way predictive information impacts on evaluative processing, particularly in tasks that employ bivalent stimulus sets. Various accounts, including framing, proactive interference, and cognitive control, appear to imply contradictory proposals on the relation between prediction and preference formation. To disambiguate whether predictive cues produce congruent biases versus opponent mechanisms in evaluative processing, we conducted two experiments in which participants were asked to rate individual food images. The image database included appetitive and aversive items. In each trial, a cue predicted, with varying degrees of reliability, the valence of the impending food image. In both experiments, we found that the ratings exhibited congruent biases as a function of the reliability of the predictive cue, with the highest evaluations following the most reliable positive-valence predictions. Eye prepositioning further showed a selective spatial bias suggestive of response preparation in line with the predictions. The response times also exhibited a pattern of results consistent with selective preparation, producing slow responses following invalid predictions. The data suggested an active form of evaluative processing, implementing a confirmation bias that aims to accommodate the prediction.

Evaluative Processing of Food Images: A Conditional Role for Viewing in Preference Formation.

Previous research suggested a role of gaze in preference formation, not merely as an expression of preference, but also as a causal influence. According to the gaze cascade hypothesis, the longer subjects look at an item, the more likely they are to develop a preference for it. However, to date the connection between viewing and liking has been investigated predominately with self-paced viewing conditions in which the subjects were required to select certain items from simultaneously presented stimuli on the basis of perceived visual attractiveness. Such conditions might promote a default, but non-mandatory connection between viewing and liking. To explore whether the connection is separable, we examined the evaluative processing of single naturalistic food images in a 2 × 2 design, conducted completely within subjects, in which we varied both the type of exposure (self-paced versus time-controlled) and the type of evaluation (non-exclusive versus exclusive). In the self-paced exclusive evaluation, longer viewing was associated with a higher likelihood of a positive evaluation. However, in the self-paced non-exclusive evaluation, the trend reversed such that longer viewing durations were associated with lesser ratings. Furthermore, in the time-controlled tasks, both with non-exclusive and exclusive evaluation, there was no significant relationship between the viewing duration and the evaluation. The overall pattern of results was consistent for viewing times measured in terms of exposure duration (i.e., the duration of stimulus presentation on the screen) and in terms of actual gaze duration (i.e., the amount of time the subject effectively gazed at the stimulus on the screen). The data indicated that viewing does not intrinsically lead to a higher evaluation when evaluating single food images; instead, the relationship between viewing duration and evaluation depends on the type of task. We suggest that self-determination of exposure duration may be a prerequisite for any influence from viewing time on evaluative processing, regardless of whether the influence is facilitative. Moreover, the purported facilitative link between viewing and liking appears to be limited to exclusive evaluation, when only a restricted number of items can be included in a chosen set.

A gaze bias with coarse spatial indexing during a gambling task.

Researchers have used eye-tracking methods to infer cognitive processes during decision making in choice tasks involving visual materials. Gaze likelihood analysis has shown a cascading effect, suggestive of a causal role for the gaze in preference formation during evaluative decision making. According to the gaze bias hypothesis, the gaze serves to build commitment gradually towards a choice. Here, we applied gaze likelihood analysis in a two-choice version of the well-known Iowa Gambling Task. This task requires active learning of the value of different choice options. As such, it does not involve visual preference formation, but choice optimization through learning. In Experiment 1 we asked subjects to choose between two decks with different payoff structures, and to give their responses using mouse clicks. Two groups of subjects were exposed to stable versus varying outcome contingencies. The analysis revealed a pronounced gaze bias towards the chosen stimuli in both groups of subjects, plateauing at more than 400 ms before the choice. The early plateauing suggested that the gaze effect partially reflected eye-hand coordination. In Experiment 2 we asked subjects to give responses using a key press. The results again showed a clear gaze bias towards the chosen deck, this time without any influence from eye-hand coordination. In both experiments, there was a clear gaze bias towards the choice even though the gaze fixations did not narrowly focus on the spatial positions of choice options. Taken together, the data suggested a role for gaze in coarse spatial indexing during non-perceptual decision making.

Influence of multiple action-outcome associations on the transition dynamics toward an optimal choice in rats.

When faced with familiar versus novel options, animals may exploit the acquired action-outcome associations or attempt to form new associations. Little is known about which factors determine the strategy of choice behavior in partially comprehended environments. Here we examine the influence of multiple action-outcome associations on choice behavior in the context of rewarding outcomes (food) and aversive outcomes (electric foot-shock). We used a nose-poke paradigm with rats, incorporating a dilemma between a familiar option and a novel, higher-value option. In Experiment 1, two groups of rats were trained with different outcome schedules: either a single action-outcome association ("Reward-Only") or dual action-outcome associations ("Reward-Shock"; with the added opportunity to avoid an electric foot-shock). In Experiment 2, we employed the same paradigm with two groups of rats performing the task under dual action-outcome associations, with different levels of threat (a low- or high-amplitude electric foot-shock). The choice behavior was clearly influenced by the action-outcome associations, with more efficient transition dynamics to the optimal choice with dual rather than single action-outcome associations. The level of threat did not affect the transition dynamics. Taken together, the data suggested that the strategy of choice behavior was modulated by the information complexity of the environment.

Women's Preference for a Male Acquaintance Enhances Social Reward Processing of Material Goods in the Anterior Cingulate Cortex.

Men, like the male of many animal species, use gifts to build satisfactory relationships with a desired woman. From the woman's perspective, all gifts are not always equally rewarding; the reward value of a gift depends on two factors: (1) the giver and (2) the type of the gift (the gift's social meaning). In this study, we investigated how these two factors interactively determine the reward value of a gift. Specifically, we examined how the neural processing for understanding a gift's social meaning is modulated by preferences for the giver. We performed a functional magnetic resonance imaging (fMRI) study in which a female participant was asked to judge a gift from a male she was acquainted with in real life. We examined the interactive effects between (1) the female participant's attitude toward the male acquaintance (liked vs. uninteresting) and (2) the type of the gift (romantic [e.g., bouquet, earrings, and perfumes] vs. non-romantic [e.g., pencils, memo pad, and moneybox]). We found that preference for an acquaintance selectively modulated activity in the anterior cingulate cortex (ACC) in response to romantic gifts, compared to non-romantic gifts. In contrast, if the woman was indifferent toward an acquaintance, no activity modulation was observed in this area for the same gifts. In addition, the ACC showed functional connectivity with the supplementary motor area/dorsal ACC (SMA/dACC), an area within the dorsal mediofrontal cortex, suggesting that it integrates action monitoring and emotional and cognitive processing in decision-making. These results suggest that attitude toward an opposite sex member has a modulatory role in recognizing the social meaning of material goods--preference for the member is a powerful modulator of social reward processing.

The deaf utilize phonological representations in visually presented verbal memory tasks.

The phonological abilities of congenitally deaf individuals are inferior to those of people who can hear. However, deaf individuals can acquire spoken languages by utilizing orthography and lip-reading. The present study used functional magnetic resonance imaging (fMRI) to show that deaf individuals utilize phonological representations via a mnemonic process. We compared the brain activation of deaf and hearing participants while they memorized serially visually presented Japanese kana letters (Kana), finger alphabets (Finger), and Arabic letters (Arabic). Hearing participants did not know which finger alphabets corresponded to which language sounds, whereas deaf participants did. All of the participants understood the correspondence between Kana and their language sounds. None of the participants knew the correspondence between Arabic and their language sounds, so this condition was used as a baseline. We found that the left superior temporal gyrus (STG) was activated by phonological representations in the deaf group when memorizing both Kana and Finger. Additionally, the brain areas associated with phonological representations for Finger in the deaf group were the same as the areas for Kana in the hearing group. Overall, despite the fact that they are superior in visual information processing, deaf individuals utilize phonological rather than visual representations in visually presented verbal memory.

Within-session dynamics of theta-gamma coupling and high-frequency oscillations during spatial alternation in rat hippocampal area CA1.

Theta-gamma coupling in the hippocampus is thought to be involved in cognitive processes. A large body of research establishes that the hippocampus plays a crucial role in the organization and maintenance of episodic memory, and that sharp-wave ripples (SWR) contribute to memory consolidation processes. Here, we investigated how the local field potentials in the hippocampal CA1 area adapted along with rats' behavioral changes within a session during a spatial alternation task that included a 1-s fixation and a 1.5-s delay. We observed that, as the session progressed, the duration from fixation onset to nose-poking in the choice hole reduced as well as the number of premature responses during the delay. Parallel with the behavioral transitions, the power of high gamma during the delay period increased whereas that of low gamma decreased later in the session. Furthermore, the strength of theta-gamma modulation later in the session showed significant increase as compared to earlier in the session. Examining SWR during the reward period, we found that the number of SWR events decreased as well as the power in a wide frequency range during SWR events. In addition, the correlation between SWR and gamma oscillations just before SWR events was higher in the earlier trials than in the later trials. Our findings support the notion that the inputs from CA3 and entorhinal cortex play a critical role in memory consolidation as well as in cognitive processes. We suggest that SWR and the inputs from the two areas serve to stabilize the task behavior and neural activities.

Theta phase shift in spike timing and modulation of gamma oscillation: a dynamic code for spatial alternation during fixation in rat hippocampal area CA1.

Although hippocampus is thought to perform various memory-related functions, little is known about the underlying dynamics of neural activity during a preparatory stage before a spatial choice. Here we focus on neural activity that reflects a memory-based code for spatial alternation, independent of current sensory and motor parameters. We recorded multiple single units and local field potentials in the stratum pyramidale of dorsal hippocampal area CA1 while rats performed a delayed spatial-alternation task. This task includes a 1-s fixation in a nose-poke port between selecting alternating reward sites and so provides time-locked enter-and-leave events. At the single-unit level, we concentrated on neurons that were specifically active during the 1-s fixation period, when the rat was ready and waiting for a cue to pursue the task. These neurons showed selective activity as a function of the alternation sequence. We observed a marked shift in the phase timing of the neuronal spikes relative to the theta oscillation, from the theta peak at the beginning of fixation to the theta trough at the end of fixation. The gamma-band local field potential also changed during the fixation period: the high-gamma power (60-90 Hz) decreased and the low-gamma power (30-45 Hz) increased toward the end. These two gamma components were observed at different phases of the ongoing theta oscillation. Taken together, our data suggest a switch in the type of information processing through the fixation period, from externally cued to internally generated.

Fear conditioning induces guinea pig auditory cortex activation by foot shock alone.

The present study used an optical imaging paradigm to investigate plastic changes in the auditory cortex induced by fear conditioning, in which a sound (conditioned stimulus, CS) was paired with an electric foot-shock (unconditioned stimulus, US). We report that, after conditioning, auditory information could be retrieved on the basis of an electric foot-shock alone. Before conditioning, the auditory cortex showed no response to a foot-shock presented in the absence of sound. In contrast, after conditioning, the mere presentation of a foot-shock without any sound succeeded in eliciting activity in the auditory cortex. Additionally, the magnitude of the optical response in the auditory cortex correlated with variation in the electrocardiogram (correlation coefficient: -0.68). The area activated in the auditory cortex, in response to the electric foot-shock, statistically significantly had a larger cross-correlation value for tone response to the CS sound (12 kHz) compared to the non-CS sounds in normal conditioning group. These results suggest that integration of different sensory modalities in the auditory cortex was established by fear conditioning.

Context and the renewal of conditioned taste aversion: the role of rat dorsal hippocampus examined by electrolytic lesion.

An extinguished conditioned response can sometimes be restored. Previous research has shown that this renewal effect depends on the context in which conditioning versus extinction takes place. Here we provide evidence that the dorsal hippocampus is critically involved in the representation of context that underscores the renewal effect. We performed electrolytic lesions in dorsal hippocampus, before or after extinction, in a conditioned taste aversion paradigm with rats. Rats that underwent all conditioning, extinction and testing procedures in the same experimental context showed no renewal during testing in the original context. In contrast, rats that underwent extinction procedures in a different experimental context than the one in which they had acquired the conditioned response, showed a reliable renewal effect during testing in the original context. When electrolytic lesion was performed prior to extinction, the context-dependent renewal effect was disrupted. When electrolytic lesion was undertaken after extinction, we observed a complex pattern of data including the blockage of the conventional renewal effect, and the appearance of an unconventional renewal effect. The implications of these results are discussed with respect to current views on the role of the dorsal hippocampus in processing context information.

A code for spatial alternation during fixation in rat hippocampal CA1 neurons.

The classical notion of hippocampal CA1 "place cells," whose activity tracks physical locations, has undergone substantial revision in recent years. Here, we provide further evidence of an abstract spatial code in hippocampal CA1, which relies on memory and adds complexity to the basic "place cell." Using a nose-poking paradigm with four male Wistar rats, we specifically concentrated on activity during fixation, when the rat was immobile and waiting for the next task event in a memory-guided spatial alternation task. The rat had to alternate between choosing the right and left holes on a trial-by-trial basis, without any sensory cue, and relying on an internal representation of the sequence of trials. Twelve tetrodes were chronically implanted for single-unit recording in the right CA1 of each rat. We focus on 76 single neurons that showed significant activation during the fixation period compared with baseline activity between trials. Among these 76 fixation neurons, we observed 38 neurons that systematically changed their fixation activity as a function of the alternation sequence. That is, even though these rats were immobile during the fixation period, the neurons fired differently for trials in which the next spatial choice should be left (i.e., RIGHT-TO-LEFT trials) compared with trials in which the next spatial choice should be right (i.e., LEFT-TO-RIGHT trials), or vice versa. Our results imply that these neurons maintain a sequential code of the required spatial response during the alternation task and thus provide abstract information, derived from memory, that can be used for efficient navigation.

Behavioral state-dependent episodic representations in rat CA1 neuronal activity during spatial alternation.

Hippocampus is considered crucial for episodic memory, as confirmed by recent findings of "episode-dependent place cells" in rodent studies, and is known to show differential activity between active exploration and quiet immobility. Most place-cell studies have focused on active periods, so the hippocampal involvement in episodic representations is less well understood. Here, we draw a typology of episode-dependent hippocampal activity among three behavioral periods, presumably governed by different molecular mechanisms: Active exploration with type 1 theta, quiet alertness with type 2 theta, and consummation with large amplitude irregular activity. Five rats were trained to perform a delayed spatial alternation task with a nose-poke paradigm and 12 tetrodes were implanted for single-unit recordings. We obtained 135 CA1 pyramidal cells and found that 75 of these fired mainly during active exploration, whereas 42 fired mainly during quiet alertness and 18 during consummation. In each type of neuron, we found episode-dependent activity: 51/75, 22/42, and 15/18, respectively. These findings extend our knowledge on the hippocampal involvement in episodic memory: Episode dependency also exists during immobile periods, and functionally dissociated cell assemblies are engaged in the maintenance of episodic information throughout different events in a task sequence.