Building compositional tasks with shared neural subspaces.

Cognition is remarkably flexible; we are able to rapidly learn and perform many different tasks1. Theoretical modeling has shown artificial neural networks trained to perform multiple tasks will re-use representations2 and computational components3 across tasks. By composing tasks from these sub-components, an agent can flexibly switch between tasks and rapidly learn new tasks4. Yet, whether such compositionality is found in the brain is unknown. Here, we show the same subspaces of neural activity represent task-relevant information across multiple tasks, with each task compositionally combining these subspaces in a task-specific manner. We trained monkeys to switch between three compositionally related tasks. Neural recordings found task-relevant information about stimulus features and motor actions were represented in subspaces of neural activity that were shared across tasks. When monkeys performed a task, neural representations in the relevant shared sensory subspace were transformed to the relevant shared motor subspace. Subspaces were flexibly engaged as monkeys discovered the task in effect; their internal belief about the current task predicted the strength of representations in task-relevant subspaces. In sum, our findings suggest that the brain can flexibly perform multiple tasks by compositionally combining task-relevant neural representations across tasks.

Automatic encoding of a target position relative to a natural scene.

We previously showed that the brain automatically represents a target position for reaching relative to a large square in the background. In the present study, we tested whether a natural scene with many complex details serves as an effective background for representing a target. In the first experiment, we used upright and inverted pictures of a natural scene. A shift of pictures significantly attenuated prism adaptation of reaching movements as long as they were upright. In one-third of participants, adaptation was almost completely cancelled whether the pictures were upright or inverted. It was remarkable that there were two distinct groups of participants, one who relies fully on the allocentric coordinate and the other who depended only when the scene was upright. In the second experiment, we examined how long it takes for a novel upright scene to serve as a background. A shift of the novel scene had no significant effects when it was presented for 500 ms before presenting a target, but significant effects were recovered when presented for 1,500 ms. These results show that a natural scene serves as a background against which a target is automatically represented once we spend 1,500 ms in the scene.NEW & NOTEWORTHY Prism adaptation of reaching was attenuated by a shift of natural scenes as long as they were upright. In one-third of participants, adaptation was fully canceled whether the scene was upright or inverted. When an upright scene was novel, it took 1,500 ms to prepare the scene for allocentric coding. These results show that a natural scene serves as a background against which a target is automatically represented once we spend 1,500 ms in the scene.

Error Signals in Motor Cortices Drive Adaptation in Reaching.

Reaching movements are subject to adaptation in response to errors induced by prisms or external perturbations. Motor cortical circuits have been hypothesized to provide execution errors that drive adaptation, but human imaging studies to date have reported that execution errors are encoded in parietal association areas. Thus, little evidence has been uncovered that supports the motor hypothesis. Here, we show that both primary motor and premotor cortices encode information on end-point errors in reaching. We further show that post-movement microstimulation to these regions caused trial-by-trial increases in errors, which subsided exponentially when the stimulation was terminated. The results indicate for the first time that motor cortical circuits provide error signals that drive trial-by-trial adaptation in reaching movements.

Modulation of prism adaptation by a shift of background in the monkey.

Recent human behavioral studies have shown that the position of a visual target is instantly represented relative to the background (e.g., a large square) and used for evaluating the error in reaching the target. In the present study, we examined whether the same allocentric mechanism is shared by the monkey. We trained two monkeys to perform a fast and accurate reaching movement toward a visual target with a square in the background. Then, a visual shift (20mm or 4.1°) was introduced by wedge prisms to examine the process of decreasing the error during an exposure period (30 trials) and the size of the error upon removal of the prisms (aftereffect). The square was shifted during each movement, either in the direction of the visual displacement or in the opposite direction, by an amount equal to the size of the visual shift. The ipsilateral shift of the background increased the asymptote during the exposure period and decreased the aftereffect, i.e., prism adaptation was attenuated by the ipsilateral shift. By contrast, a contralateral shift enhanced adaptation. We further tested whether the shift of the square alone could cause an increase in the motor error. Although the target did not move, the shift of the square increased the motor error in the direction of the shift. These results were generally consistent with the results reported in human subjects, suggesting that the monkey and the human share the same neural mechanisms for representing a target relative to the background.

Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration.

Cerebellar damage can profoundly impair human motor adaptation. For example, if reaching movements are perturbed abruptly, cerebellar damage impairs the ability to learn from the perturbation-induced errors. Interestingly, if the perturbation is imposed gradually over many trials, people with cerebellar damage may exhibit improved adaptation. However, this result is controversial, since the differential effects of gradual vs. abrupt protocols have not been observed in all studies. To examine this question, we recruited patients with pure cerebellar ataxia due to cerebellar cortical atrophy (n = 13) and asked them to reach to a target while viewing the scene through wedge prisms. The prisms were computer controlled, making it possible to impose the full perturbation abruptly in one trial, or build up the perturbation gradually over many trials. To control visual feedback, we employed shutter glasses that removed visual feedback during the reach, allowing us to measure trial-by-trial learning from error (termed error-sensitivity), and trial-by-trial decay of motor memory (termed forgetting). We found that the patients benefited significantly from the gradual protocol, improving their performance with respect to the abrupt protocol by exhibiting smaller errors during the exposure block, and producing larger aftereffects during the postexposure block. Trial-by-trial analysis suggested that this improvement was due to increased error-sensitivity in the gradual protocol. Therefore, cerebellar patients exhibited an improved ability to learn from error if they experienced those errors gradually. This improvement coincided with increased error-sensitivity and was present in both groups of subjects, suggesting that control of error-sensitivity may be spared despite cerebellar damage.

Automatic representation of a visual stimulus relative to a background in the right precuneus.

Our brains represent the position of a visual stimulus egocentrically, in either retinal or craniotopic coordinates. In addition, recent behavioral studies have shown that the stimulus position is automatically represented allocentrically relative to a large frame in the background. Here, we investigated neural correlates of the 'background coordinate' using an fMRI adaptation technique. A red dot was presented at different locations on a screen, in combination with a rectangular frame that was also presented at different locations, while the participants looked at a fixation cross. When the red dot was presented repeatedly at the same location relative to the rectangular frame, the fMRI signals significantly decreased in the right precuneus. No adaptation was observed after repeated presentations relative to a small, but salient, landmark. These results suggest that the background coordinate is implemented in the right precuneus.

Three timescales in prism adaptation.

It has been proposed that motor adaptation depends on at least two learning systems, one that learns fast but with poor retention and another that learns slowly but with better retention (Smith MA, Ghazizadeh A, Shadmehr R. PLoS Biol 4: e179, 2006). This two-state model has been shown to account for a range of behavior in the force field adaptation task. In the present study, we examined whether such a two-state model could also account for behavior arising from adaptation to a prismatic displacement of the visual field. We first confirmed that an "adaptation rebound," a critical prediction of the two-state model, occurred when visual feedback was deprived after an adaptation-extinction episode. We then examined the speed of decay of the prism aftereffect (without any visual feedback) after repetitions of 30, 150, and 500 trials of prism exposure. The speed of decay decreased with the number of exposure trials, a phenomenon that was best explained by assuming an "ultraslow" system, in addition to the fast and slow systems. Finally, we compared retention of aftereffects 24 h after 150 or 500 trials of exposure: retention was significantly greater after 500 than 150 trials. This difference in retention could not be explained by the two-state model but was well explained by the three-state model as arising from the difference in the amount of adaptation of the "ultraslow process." These results suggest that there are not only fast and slow systems but also an ultraslow learning system in prism adaptation that is activated by prolonged prism exposure of 150-500 trials.

Cancelling prism adaptation by a shift of background: a novel utility of allocentric coordinates for extracting motor errors.

Many previous studies have reported that our brains are able to encode a target position not only in body-centered coordinates but also in terms of landmarks in the background. The importance of such allocentric memory increases when we are forced to complete a delayed reaching task after the target has disappeared. However, the merit of allocentric memory in natural situations in which we are free to make an immediate reach toward a target has remained elusive. We hypothesized that allocentric memory is essential even in an immediate reach for dissociating between error attributable to the motor system and error attributable to target motion. We show here in humans that prism adaptation, that is, adaptation of reaching movements in response to errors attributable to displacement of the visual field, can be cancelled or enhanced simply by moving the background in mid-flight of the reaching movement. The results provide direct evidence for the novel contribution of allocentric memory in providing information on "where I intended to go," thereby discriminating the effect of target motion from the error resulting from the issued motor control signals.

Activation of cholecystokinin neurons in the dorsal pallium of the telencephalon is indispensable for the acquisition of chick imprinting behavior.

Chick imprinting behavior is a good model for the study of learning and memory. Imprinting object is recognized and processed in the visual wulst, and the memory is stored in the intermediate medial mesopallium in the dorsal pallium of the telencephalon. We identified chicken cholecystokinin (CCK)-expressing cells localized in these area. The number of CCK mRNA-positive cells increased in chicks underwent imprinting training, and these cells expressed nuclear Fos immunoreactivity at high frequency in these regions. Most of these CCK-positive cells were glutamatergic and negative for parvalbumin immunoreactivity. Semi-quantitative PCR analysis revealed that the CCK mRNA levels were significantly increased in the trained chicks compared with untrained chicks. In contrast, the increase in CCK- and c-Fos-double-positive cells associated with the training was not observed after closure of the critical period. These results indicate that CCK cells in the dorsal pallium are activated acutely by visual training that can elicit imprinting. In addition, the CCK receptor antagonist significantly suppressed the acquisition of memory. These results suggest that the activation of CCK cells in the visual wulst as well as in the intermediate medial mesopallium by visual stimuli is indispensable for the acquisition of visual imprinting.

Imprinting modulates processing of visual information in the visual wulst of chicks.

BACKGROUND: Imprinting behavior is one form of learning and memory in precocial birds. With the aim of elucidating of the neural basis for visual imprinting, we focused on visual information processing. RESULTS: A lesion in the visual wulst, which is similar functionally to the mammalian visual cortex, caused anterograde amnesia in visual imprinting behavior. Since the color of an object was one of the important cues for imprinting, we investigated color information processing in the visual wulst. Intrinsic optical signals from the visual wulst were detected in the early posthatch period and the peak regions of responses to red, green, and blue were spatially organized from the caudal to the nasal regions in dark-reared chicks. This spatial representation of color recognition showed plastic changes, and the response pattern along the antero-posterior axis of the visual wulst altered according to the color the chick was imprinted to. CONCLUSION: These results indicate that the thalamofugal pathway is critical for learning the imprinting stimulus and that the visual wulst shows learning-related plasticity and may relay processed visual information to indicate the color of the imprint stimulus to the memory storage region, e.g., the intermediate medial mesopallium.