An intra-oral flavor detection task in freely moving mice.

Flavor plays a critical role in the pleasure of food. Flavor research has mainly focused on human subjects and revealed that many brain regions are involved in flavor perception. However, animal models for elucidating the mechanisms of neural circuits are lacking. Herein, we demonstrate the use of a novel behavioral task in which mice are capable of flavor detection. When the olfactory pathways of the mice were blocked, they could not perform the task. However, behavioral accuracy was not affected when the gustatory pathway was blocked by benzocaine. These results indicate that the mice performed this detection task mainly based on the olfaction. We conclude that this novel task can contribute to research on the neural mechanisms of flavor perception.

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.

Bi-directional encoding of context-based odors and behavioral states by the nucleus of the lateral olfactory tract.

The nucleus of the lateral olfactory tract (NLOT) is not only a part of the olfactory cortex that receives olfactory sensory inputs but also a part of the cortical amygdala, which regulates motivational behaviors. To examine how neural activity of the NLOT is modulated by decision-making processes that occur during various states of learned goal-directed behaviors, we recorded NLOT spike activities of mice performing odor-guided go/no-go tasks to obtain a water reward. We observed that several NLOT neurons exhibited sharp go-cue excitation and persistent no-go-cue suppression responses triggered by an odor onset. The bidirectional cue encoding introduced NLOT population response dynamics and provided a high odor decoding accuracy before executing cue-odor-evoked behaviors. The go-cue responsive neurons were also activated in the reward drinking state, indicating context-based odor-outcome associations. These findings suggest that NLOT neurons play an important role in the translation from context-based odor information to appropriate behavior.

Contribution of non-sensory neurons in visual cortical areas to visually guided decisions in the rat.

It is widely assumed that trial-by-trial variability in visual detection performance is explained by the fidelity of visual responses in visual cortical areas influenced by fluctuations of internal states, such as vigilance and behavioral history. However, it is not clear which neuronal ensembles represent such different internal states. Here, we utilized a visual detection task, which distinguishes internal states in response to identical stimuli, while recording neurons simultaneously from the primary visual cortex (V1) and the posterior parietal cortex (PPC). We found that rats sometimes withheld their responses to visual stimuli despite the robust presence of visual responses in V1. Our unsupervised analysis revealed distinct population dynamics segregating hit responses from misses, orthogonally embedded to visual response dynamics in both V1 and PPC. Heterogeneous non-sensory neurons in V1 and PPC significantly contributed to population-level encoding accompanied with the modulation of noise correlation only in V1. These results highlight the non-trivial contributions of non-sensory neurons in V1 and PPC for population-level computations that reflect the animals' internal states to drive behavioral responses to visual stimuli.

Tuning of olfactory cortex ventral tenia tecta neurons to distinct task elements of goal-directed behavior.

The ventral tenia tecta (vTT) is a component of the olfactory cortex and receives both bottom-up odor signals and top-down signals. However, the roles of the vTT in odor-coding and integration of inputs are poorly understood. Here, we investigated the involvement of the vTT in these processes by recording the activity from individual vTT neurons during the performance of learned odor-guided reward-directed tasks in mice. We report that individual vTT cells are highly tuned to a specific behavioral epoch of learned tasks, whereby the duration of increased firing correlated with the temporal length of the behavioral epoch. The peak time for increased firing among recorded vTT cells encompassed almost the entire temporal window of the tasks. Collectively, our results indicate that vTT cells are selectively activated during a specific behavioral context and that the function of the vTT changes dynamically in a context-dependent manner during goal-directed behaviors.