It is generally believed that the hippocampus plays a crucial role in declarative memory—remembering facts and events—but not in gradual stimulus-response association or incremental value learning. Based on the finding that CA1 conveys strong value signals during dynamic foraging, we investigated the possibility that the hippocampus contributes to incremental value learning. Specifically, we examined effects of inactivating different subregions of the dorsal hippocampus on behavioral performance of mice performing a dynamic foraging task in a modified T-maze. A reinforcement learning model-based analysis indicated that inactivation of CA1, but not dentate gyrus, CA3, or CA2, impaired trial-by-trial updating of chosen value without affecting value-dependent action selection. As a result, it took longer for CA1-inactivated mice to bias their choices toward the higher-reward-probability target after changes in reward probability. Our results indicate, contrary to the traditional view, that the hippocampus, especially CA1, might contribute to incremental value learning under certain circumstances.

No abstract

Strong hippocampal mossy fiber synapses are thought to function as detonators, imposing “teaching” signals onto CA3 neurons during new memory formation. For an empirical test of this long‐standing view, we examined effects of optogenetically stimulating mossy fibers on spatial firing of CA3 neurons in freely‐moving mice. We found that spatially restricted mossy fiber stimulation drives novel place‐specific firing in some CA3 pyramidal neurons. Such neurons comprise only a minority, however, and many more CA3 neurons showed inhibited spatial firing during mossy fiber stimulation. Also, changes in spatial firing induced by mossy fiber stimulation, both activated and inhibited, reverted immediately upon stimulation termination, leaving CA3 place fields unaltered. Our results do not support the traditional view that mossy fibers impose teaching signals onto CA3 network, and show robustness of established CA3 spatial representations.

Strong hippocampal mossy fiber synapses are thought to function as detonators, imposing 'teaching' signals onto CA3 neurons during new memory formation. For an empirical test of this long-standing view, we examined effects of stimulating mossy fibers on spatial firing of CA3 neurons in freely-moving mice. We found that optogenetic stimulation of mossy fibers can alter CA3 spatial firing, but their effects are only transient. Spatially restricted mossy fiber stimulation, either congruent or incongruent with CA3 place fields, was more likely to suppress than enhance CA3 neuronal activity. Also, changes in spatial firing induced by optogenetic stimulation reverted immediately upon stimulation termination, leaving CA3 place fields unaltered. Our results do not support the traditional view that mossy fibers impose teaching signals onto CA3 network, and show robustness of established CA3 spatial representations.

The ability to process and act upon incoming sounds during locomotion is critical for survival. Intriguingly, sound responses of auditory cortical neurons are on average weaker during locomotion as compared to immobility and these results have been suggested to reflect a computational resource allocation shift from auditory to visual processing. However, the evolutionary benefit of this hypothesis remains unclear. In particular, whether weaker sound-evoked responses during locomotion indeed reflect a reduced involvement of the auditory cortex, or whether they result from an alternative neural computation in this state remains unresolved. To address this question, we first used neural inactivation in behaving mice and found that the auditory cortex plays a critical role in sound-guided behavior during locomotion. To investigate the nature of this processing, we used two-photon calcium imaging of local excitatory auditory cortical neural populations in awake mice. We found that underlying a net inhibitory effect of locomotion on sound-evoked response magnitude, spatially intermingled neuronal subpopulations were differentially influenced by locomotion. Further, the net inhibitory effect of locomotion on sound-evoked responses was strongly shaped by elevated ongoing activity. Importantly, rather than reflecting enhanced “noise”, this ongoing activity reliably encoded the animal’s locomotion speed. Prediction analyses revealed that sound, locomotive state and their integration are strongly encoded by auditory cortical ensemble activity. Finally, we found consistent patterns of locomotion-sound integration in electrophysiologically recorded activity in freely moving rats. Together, our data suggest that auditory cortical ensembles are not simply suppressed by locomotion but rather encode it alongside sound information to support sound perception during locomotion.

Hippocampal mossy fibers have long been proposed to impose new patterns to learn onto CA3 neurons during new memory formation. However, inconsistent with this theory, we found in our previous study that mossy fiber stimulation induces only transient changes in CA3 spatial firing in a familiar environment. Here, we tested whether mossy fiber stimulation affects CA3 spatial firing differently between familiar and novel environments. We compared spatial firing of CA3 neurons before and after optogenetic stimulation of mossy fibers in freely behaving mice in a familiar and three sets of novel environments. We found that CA3 neurons are more responsive to mossy fiber stimulation in the novel than familiar environments. However, we failed to obtain evidence for long‐lasting effect of mossy fiber stimulation on spatial firing of CA3 neurons in both the familiar and novel environments. Our results provide further evidence against the view that mossy fibers carry teaching signals.