Effective modulation from the ventral medial to the dorsal medial portion of the prefrontal cortex in memory confidence-based behavioral control.

Metacognition includes the ability to refer to one's own cognitive states, such as confidence, and adaptively control behavior based on this information. This ability is thought to allow us to predictably control our behavior without external feedback, for example, even before we take action. Many studies have suggested that metacognition requires a brain-wide network of multiple brain regions. However, the modulation of effective connectivity within this network during metacognitive tasks remains unclear. This study focused on medial prefrontal regions, which have recently been suggested to be particularly involved in metacognition. We examined whether modulation of effective connectivity specific to metacognitive behavioral control is observed using model-based network analysis and dynamic causal modeling (DCM). The results showed that negative modulation from the ventral medial prefrontal cortex to the dorsal medial prefrontal cortex was observed in situations that required metacognitive behavioral control but not in situations that did not require such metacognitive control. Furthermore, this modulation was particularly pronounced in the group of participants who could better use metacognition for behavioral control. These results imply hierarchical properties of metacognition-related brain networks.

Rats adaptively seek information to accommodate a lack of information.

Metacognition is the ability to adaptively control one's behavior by referring to one's own cognitive processes. It is thought to contribute to learning in situations where there is insufficient information available from the environment. Information-seeking behavior is a type of metacognition in which one confirms the necessary information only when one does not have the necessary and sufficient information to accomplish a task. The rats were required to respond to a nose poke hole on one wall of the experimental box for a certain period of time and then move to the opposite side at a specific time. Unfortunately, they were unable to match the timing when responding to the hole on one side. Therefore, they had to look back and confirm that now was the right time. The results obtained by analyzing these looking-back movements using a motion capture system showed that this behavior occurred frequently and rapidly in situations of insufficient information, such as in the early stages of learning, but was hardly observed and became slower as learning progressed. These results suggest that rats can adjust their behavior in response to a lack of information more flexibly than previously assumed.

Auditory Cortex Neurons Show Task-Related and Learning-Dependent Selectivity toward Sensory Input and Reward during the Learning Process of an Associative Memory Task.

The activity of primary auditory cortex (A1) neurons is modulated not only by sensory inputs but also by other task-related variables in associative learning. However, it is unclear how A1 neural activity changes dynamically in response to these variables during the learning process of associative memory tasks. Therefore, we developed an associative memory task using auditory stimuli in rats. In this task, rats were required to associate tone frequencies (high and low) with a choice of ports (right or left) to obtain a reward. The activity of A1 neurons in the rats during the learning process of the task was recorded. A1 neurons increased their firing rates either when the rats were presented with a high or low tone (frequency-selective cells) before they chose either the left or right port (choice-direction cells), or when they received a reward after choosing either the left or right port (reward-direction cells). Furthermore, the proportion of frequency-selective cells and reward-direction cells increased with task acquisition and reached the maximum level in the last stage of learning. These results suggest that A1 neurons have task- and learning-dependent selectivity toward sensory input and reward when auditory tones and behavioral responses are gradually associated during task training. This selective activity of A1 neurons may facilitate the formation of associations, leading to the consolidation of associative memory.

Hippocampal CA1 Neurons Represent Positive Feedback During the Learning Process of an Associative Memory Task.

The hippocampus is crucial for forming associations between environmental stimuli. However, it is unclear how neural activities of hippocampal neurons dynamically change during the learning process. To address this question, we developed an associative memory task for rats with auditory stimuli. In this task, the rats were required to associate tone pitches (high and low) and ports (right and left) to obtain a reward. We recorded the firing activity of neurons in rats hippocampal CA1 during the learning process of the task. As a result, many hippocampal CA1 neurons increased their firing rates when the rats received a reward after choosing either the left or right port. We referred to these cells as "reward-direction cells." Furthermore, the proportion of the reward-direction cells increased in the middle-stage of learning but decreased after the completion of learning. This result suggests that the activity of reward-direction cells might serve as "positive feedback" signal that facilitates the formation of associations between tone pitches and port choice.

Production of regular rhythm induced by external stimuli in rats.

Rhythmic ability is important for locomotion, communication, and coordination between group members during the daily life of animals. We aimed to examine the rhythm perception and production abilities in rats within the range of a subsecond to a few seconds. We trained rats to respond to audio-visual stimuli presented in regular, isochronous rhythms at six time-intervals (0.5-2 s). Five out of six rats successfully learned to respond to the sequential stimuli. All subjects showed periodic actions. The actions to regular stimuli were faster than randomly presented stimuli in the medium-tempo conditions. In slower and faster tempo conditions, the actions of some subjects were not periodic or phase-matched to the stimuli. The asynchrony regarding the stimulus onset became larger or smaller when the last stimulus of the sequence was presented at deviated timings. Thus, the actions of the rats were tempo matched to the regular rhythm, but not completely anticipative. We also compared the extent of phase-matching and variability of rhythm production among the interval conditions. In interval conditions longer than 1.5 s, variability tended to be larger. In conclusion, rats showed a tempo matching ability to regular rhythms to a certain degree, but maintenance of a constant tempo to slower rhythm conditions was difficult. Our findings suggest that non-vocal learning mammals have the potential to produce flexible rhythms in subsecond timing.

Dynamics of memory engrams.

In this update article, we focus on "memory engrams", which are traces of long-term memory in the brain, and emphasizes that they are not static but dynamic. We first introduce the major findings in neuroscience and psychology reporting that memory engrams are sometimes diffuse and unstable, indicating that they are dynamically modified processes of consolidation and reconsolidation. Second, we introduce and discuss the concepts of cell assembly and engram cell, the former has been investigated by psychological experiments and behavioral electrophysiology and the latter is defined by recent combination of activity-dependent cell labelling with optogenetics to show causal relationships between cell population activity and behavioral changes. Third, we discuss the similarities and differences between the cell assembly and engram cell concepts to reveal the dynamics of memory engrams. We also discuss the advantages and problems of live-cell imaging, which has recently been developed to visualize multineuronal activities. The last section suggests the experimental strategy and background assumptions for future research of memory engrams. The former encourages recording of cell assemblies from different brain regions during memory consolidation-reconsolidation processes, while the latter emphasizes the multipotentiality of neurons and regions that contribute to dynamics of memory engrams in the working brain.

Regulation of action selection based on metacognition in humans via a ventral and dorsal medial prefrontal cortical network.

Metacognition is defined as cognition about one's own cognitive state; it enables us to estimate our own performance during goal-directed actions and to select a suitable strategy based on that estimation. Identifying the neural mechanisms that underlie this process will contribute to our understanding of how we realize adaptive self-control in daily life. Here, we focused on the neural substrates that allow us to voluntarily utilize prospective metacognition to carry out such action selection. Participants were asked to bet on their recall of sound stimuli presented at an earlier time in a delayed match-to-sample task of rapidly changing sound stimuli. During the task, brain activity was measured using functional magnetic resonance imaging. We found that the brain network composed of the ventral and dorsal parts of the medial prefrontal cortex and the medial precuneus regulated the strategic selection of risk/return profiles based on metacognition. In particular, increments in functional connectivity between the ventral and dorsal medial prefrontal cortices during high-risk/return bets correlated with the adaptiveness of the bet (as measured by the correspondence between choosing high risk/return bets and high accuracy of task performance). This index is considered to reflect the degree of voluntary use of metacognition to bet. These findings suggest that the strong connectivity within the network involving the ventral and dorsal medial prefrontal cortices enables us to utilize metacognition to select actions for achieving a goal efficiently.

Rats show adaptive choice in a metacognitive task with high uncertainty.

Metacognition refers to the use of one's cognitive processes to coordinate behavior. Many higher cognitive functions such as feeling-of-knowing judgment and theory of mind are thought to be metacognitive processes. Although some primate species also show this ability in the form of behavioral control, a rodent model of metacognition is required for advanced studies of this phenomenon at behavioral, molecular, and neural levels. Here we show that rats could reliably be trained in a metacognitive task. The rats were trained to remember the location of a nose-poke hole and later indicate the location via a behavioral task. Rats had options of either demonstrating their memory or switching to an easier task (escape). Four rats were used in a two-choice metacognitive task, and 3 were used in a six-choice task. In the six-choice task, rats increased the likelihood of receiving a reward by utilizing the option to escape, in exchange for a decrease in the amount of reward received per correct trial. Furthermore, rats escaped more in sample-omitted trials than in standard trials. Results are consistent with the hypothesis that rats have metacognition, and could be utilized as a benchmark for further metacognition studies in rats. However, rats in the two-choice task did not use the escape response adaptively. These results were consistent with those seen in capuchin monkeys. Similarity between rodents and primates in task switching should expand the possibility of comparative studies of metacognition. (PsycINFO Database Record

Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion.

Emotional contagion occurs when an individual acquires the emotional state of another via social cues, and is an important component of empathy. Empathic responses seen in rodents are often explained by emotional contagion. Rats emit 50kHz ultrasonic vocalizations (USVs) in positive contexts, and emit 22kHz USVs in negative contexts. We tested whether rats show positive or negative emotional contagion after hearing conspecific USVs via a cognitive bias task. We hypothesized that animals in positive emotional states would perceive an ambiguous cue as being good (optimistic bias) whereas animals in negative states would perceive the same cue as being bad (pessimistic bias). Rats were trained to respond differently to two sounds with distinct pitches, each of which signaled either a positive or a negative outcome. An ambiguous cue with a frequency falling between the two stimuli tested whether rats interpreted it as positive or negative. Results showed that rats responded to ambiguous cues as positive when they heard the 50kHz USV (positive vocalizations) and negative when they heard the 22kHz USV (negative vocalizations). This suggests that conspecific USVs can evoke emotional contagion, both for positive and negative emotions, to change the affective states in receivers.

Relatively high motivation for context-evoked reward produces the magnitude effect in rats.

Using a concurrent-chain schedule, we demonstrated the effect of absolute reinforcement (i.e., the magnitude effect) on choice behavior in rats. In general, animals' simultaneous choices conform to a relative reinforcement ratio between alternatives. However, studies in pigeons and rats have found that on a concurrent-chain schedule, the overall reinforcement ratio, or absolute amount, also influences choice. The effect of reinforcement amount has also been studied in inter-temporal choice situations, and this effect has been referred to as the magnitude effect. The magnitude effect has been observed in humans under various conditions, but little research has assessed it in animals (e.g., pigeons and rats). The present study confirmed the effect of reinforcement amount in rats during simultaneous and inter-temporal choice situations. We used a concurrent-chain procedure to examine the cause of the magnitude effect during inter-temporal choice. Our results suggest that rats can use differences in reinforcement amount as a contextual cue during choice, and the direction of the magnitude effect in rats might be similar to humans when using the present procedure. Furthermore, our results indicate that the magnitude effect was caused by the initial-link effect when the reinforcement amount was relatively small, while a loss aversion tendency was observed when the reinforcement amount changed within a session. The emergence of the initial-link effect and loss aversion suggests that rats make choices through cognitive processes predicted by prospect theory.