The behavioral signature of stepwise learning strategy in male rats and its neural correlate in the basal forebrain.

Studies of associative learning have commonly focused on how rewarding outcomes are predicted by either sensory stimuli or animals' actions. However, in many learning scenarios, reward delivery requires the occurrence of both sensory stimuli and animals' actions in a specific order, in the form of behavioral sequences. How such behavioral sequences are learned is much less understood. Here we provide behavioral and neurophysiological evidence to show that behavioral sequences are learned using a stepwise strategy. In male rats learning a new association, learning started from the behavioral event closest to the reward and sequentially incorporated earlier events. This led to the sequential refinement of reward-seeking behaviors, which was characterized by the stepwise elimination of ineffective and non-rewarded behavioral sequences. At the neuronal level, this stepwise learning process was mirrored by the sequential emergence of basal forebrain neuronal responses toward each event, which quantitatively conveyed a reward prediction error signal and promoted reward-seeking behaviors. Together, these behavioral and neural signatures revealed how behavioral sequences were learned in discrete steps and when each learning step took place.

Synchronization across sensory cortical areas by electrical microstimulation is sufficient for behavioral discrimination.

The temporal correlation hypothesis proposes that cortical neurons engage in synchronized activity, thus configuring a general mechanism to account for a range of cognitive processes from perceptual binding to consciousness. However, most studies supporting this hypothesis have only provided correlational, but not causal evidence. Here, we used electrical microstimulation of the visual and somatosensory cortices of the rat in both hemispheres, to test whether rats could discriminate synchronous versus asynchronous patterns of stimulation applied to the same cortical sites. To disambiguate synchrony from other related parameters, our experiments independently manipulated the rate and intensity of stimulation, the spatial locations of stimulation, the exact temporal sequence of stimulation patterns, and the degree of synchrony across stimulation sites. We found that rats reliably distinguished between 2 microstimulation patterns, differing in the spatial arrangement of cortical sites stimulated synchronously. Also, their performance was proportional to the level of synchrony in the microstimulation patterns. We demonstrated that rats can recognize artificial current patterns containing precise synchronization features, thus providing the first direct evidence that artificial synchronous activity can guide behavior. Such precise temporal information can be used as feedback signals in machine interface arrangements.