No abstract

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.

Cortical neurons show distinct firing patterns across multiple task epochs characterized by different computations. Recent studies suggest that such distinct patterns underlie dynamic population code achieving computational flexibility, whereas neurons in some cortical areas often show coherent firing patterns across epochs. To understand how coherent single-neuron code contributes to dynamic population code, we analyzed neural responses in the rat perirhinal cortex (PRC) during cue and reward epochs of a two-alternative forced-choice task. We found that the PRC neurons often encoded the opposite choice directions between those epochs. By using principal component analysis as a population-level analysis, we identified neural subspaces associated with each epoch, which reflected coordination across the neurons. The cue and reward epochs shared neural dimensions where the choice directions were consistently discriminated. Interestingly, those dimensions were supported by dynamically changing contributions of the individual neurons. These results demonstrated heterogeneity of coherent single-neuron representations in their contributions to population code.

13 14 Cortical neurons show distinct firing patterns across multiple task-epochs 15 characterized by distinct computational aspects. Recent studies suggest that 16 such distinct patterns underly dynamic population code achieving 17 computational flexibility, whereas neurons in some cortical areas often show 18 coherent firing patterns across epochs. To understand how such coherent 19 single-neuron code contribute to dynamic population code, we analyzed 20 neural responses in the perirhinal cortex (PRC) during cue and reward 21 epochs of a two-alternative forced-choice task. We found that the PRC 22 neurons often encoded the opposite choice-directions between those epochs. 23 By using principal component analysis as population-level analysis, we 24 identified neural subspaces associated with each epoch, which reflected 25 coordinated patterns across the neurons. The cue and reward epochs shared 26 neural dimensions where the choice directions were consistently 27 discriminated. Interestingly, those dimensions were supported by 28 dynamically changing contributions of individual neurons. These results 29 indicated heterogeneity of coherent single-neuron responses in their 30 3 contribution to population code. 31 32 33 65 two-alternative forced-choice task and analyzed neural responses in two 66 5 epochs, where different computations are demanded: making predictions 67 about the outcome of choices (cue epoch) and reinforcing the choices (reward 68 epoch). By taking advantage of the interleaved visual and olfactory cue 69 stimuli, which allowed us to evaluate modality-independent encodings, we 70 analyzed dynamic population encodings related to different choices during 71 those epochs in relation to single-neuron level selectivity. 72 73 74 Results 75 76Neurons in the PRC encode choice directions during a two-alternative 77 forced-choice task. We trained rats to perform a two-alternative forced-78 choice task where they chose a target port (left/right) associated with a 79 presented cue to obtain reward ( Fig. 1a-b). The task performance was of a 80 similar level regardless of the cue modality (mean correct rate in visual 81 trials = 95.6 ± 5.5%; olfactory trials = 92.3 ± 4.3%). We recorded spiking 82 activities from the left PRC (n = 207 neurons) during the task performance 83 (37 sessions in five rats). 84 6 As shown in Fig. 1c, the PRC neurons typically showed distinct temporal 85 firing patterns in left and right trials. To characterize how the PRC was 86 activated by different trial conditions, we compared firing pattens among 87 different cue-modalities and choices across all the recorded neurons. The 88 neurons were sorted by their peak firing rates in visually-cued left choice 89 trials (top left in Fig. 1d). As consistent with previous studies in other brain 90 regions 28-33 , the peak responses of the PRC neurons tiled the duration of a 91 trial. The response patterns across the neurons were well preserved 92 between the cue modalities but much less so between the choice directions 93 (comparison between th...