Muneyoshi Takahashi

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.

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.

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.

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.

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.

Transition Dynamics in Spatial Choice

Previous research has provided abundant evidence that negative as well as positive reinforcers can elicit operant responding in rats. Less is known, however, about the relative impact of positive versus negative reinforcers on the dynamics of spatial choice in a complex setting, including old and new stimuli. To study such dynamics, we devised a behavioral paradigm consisting of an initial learning phase, followed by a “transition test,” which included a novel stimulus. In the initial learning phase, rats acquired an operant nose-poke response to a visual (LED) onset at the central hole in the front wall of a Skinner box. We trained two groups of rats, with different types of reinforcement; Group 1(appetitive learning) obtained a food pellet as reinforcement for correct responding, whereas Group 2 (appetitive and avoidance learning) obtained a food pellet and avoided a foot shock as reinforcement for correct responding. Once both groups had established similar, near-perfect levels of performance, we introduced a first transition test, in which a second visual (LED) onset was presented simultaneously with the visual onset at the center. The rats were free to continue responding to the central hole (with the same reinforcement schedule for central responding as during the initial learning). However, the rats obtained three instead of only one food pellet for responding to the peripheral hole (Group 1 and Group 2) as well as avoiding a foot shock (Group 2). Overall, as compared to rats in Group 1, the rats that underwent both appetitive and avoidance learning showed more efficient transition, switching to peripheral responding. These data cannot easily be accommodated by operant conditioning models, according to which the rats in Group 2 should have been particularly motivated to continue responding at the central hole. Instead, we propose that their spatial choice was modified by a complex interaction of classic and operant learning.

The Theta Cycle and Spike Timing During Fixation in Rat Hippocampal CA1

In this paper, we report the first evidence that the spikes of CA1 neurons shift approximately half of the theta cycle: The shift occurs from the positive peak of the cycle recorded in the CA1 cell layer at the beginning of fixation, to the negative trough at the end of fixation. This happens during a one-second period of immobile fixation, while the rat is fully alert and waits for the next event. It is known that the strongest input from entorhinal cortex occurs at the positive peak of the CA1 cell layer theta, whereas the strongest input from CA3 is associated with the trough of the theta. We hypothesize that CA1 pyramidal cells perform a function as an adaptive filter between entorhinal cortex and CA3, propagating relevant information depending on task requirements.

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.

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

Abstract 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.