Goal-seeking compresses neural codes for space in the human hippocampus and orbitofrontal cortex.

Humans can navigate flexibly to meet their goals. Here, we asked how the neural representation of allocentric space is distorted by goal-directed behavior. Participants navigated an agent to two successive goal locations in a grid world environment comprising four interlinked rooms, with a contextual cue indicating the conditional dependence of one goal location on another. Examining the neural geometry by which room and context were encoded in fMRI signals, we found that map-like representations of the environment emerged in both hippocampus and neocortex. Cognitive maps in hippocampus and orbitofrontal cortices were compressed so that locations cued as goals were coded together in neural state space, and these distortions predicted successful learning. This effect was captured by a computational model in which current and prospective locations are jointly encoded in a place code, providing a theory of how goals warp the neural representation of space in macroscopic neural signals.

An implicit memory of errors limits human sensorimotor adaptation.

During extended motor adaptation, learning appears to saturate despite persistence of residual errors. This adaptation limit is not fixed but varies with perturbation variance; when variance is high, residual errors become larger. These changes in total adaptation could relate to either implicit or explicit learning systems. Here, we found that when adaptation relied solely on the explicit system, residual errors disappeared and learning was unaltered by perturbation variability. In contrast, when learning depended entirely, or in part, on implicit learning, residual errors reappeared. Total implicit adaptation decreased in the high-variance environment due to changes in error sensitivity, not in forgetting. These observations suggest a model in which the implicit system becomes more sensitive to errors when they occur in a consistent direction. Thus, residual errors in motor adaptation are at least in part caused by an implicit learning system that modulates its error sensitivity in response to the consistency of past errors.

Neural state space alignment for magnitude generalization in humans and recurrent networks.

A prerequisite for intelligent behavior is to understand how stimuli are related and to generalize this knowledge across contexts. Generalization can be challenging when relational patterns are shared across contexts but exist on different physical scales. Here, we studied neural representations in humans and recurrent neural networks performing a magnitude comparison task, for which it was advantageous to generalize concepts of "more" or "less" between contexts. Using multivariate analysis of human brain signals and of neural network hidden unit activity, we observed that both systems developed parallel neural "number lines" for each context. In both model systems, these number state spaces were aligned in a way that explicitly facilitated generalization of relational concepts (more and less). These findings suggest a previously overlooked role for neural normalization in supporting transfer of a simple form of abstract relational knowledge (magnitude) in humans and machine learning systems.

Structure learning and the posterior parietal cortex.

We propose a theory of structure learning in the primate brain. We argue that the parietal cortex is critical for learning about relations among the objects and categories that populate a visual scene. We suggest that current deep learning models exhibit poor global scene understanding because they fail to perform the relational inferences that occur in the primate dorsal stream. We review studies of neural coding in primate posterior parietal cortex (PPC), drawing the conclusion that neurons in this brain area represent potentially high-dimensional inputs on a low-dimensional manifold that encodes the relative position of objects or features in physical space, and relations among entities in abstract conceptual space. We argue that this low-dimensional code supports generalisation of relational information, even in nonspatial domains. Finally, we propose that structure learning is grounded in the actions that primates take when they reach for objects or fixate them with their eyes. We sketch a model of how this might occur in neural circuits.

The visual geometry of a tool modulates generalization during adaptation.

Knowledge about a tool's dynamics can be acquired from the visual configuration of the tool and through physical interaction. Here, we examine how visual information affects the generalization of dynamic learning during tool use. Subjects rotated a virtual hammer-like object while we varied the object dynamics separately for two rotational directions. This allowed us to quantify the coupling of adaptation between the directions, that is, how adaptation transferred from one direction to the other. Two groups experienced the same dynamics of the object. For one group, the object's visual configuration was displayed, while for the other, the visual display was uninformative as to the dynamics. We fit a range of context-dependent state-space models to the data, comparing different forms of coupling. We found that when the object's visual configuration was explicitly provided, there was substantial coupling, such that 31% of learning in one direction transferred to the other. In contrast, when the visual configuration was ambiguous, despite experiencing the same dynamics, the coupling was reduced to 12%. Our results suggest that generalization of dynamic learning of a tool relies, not only on its dynamic behaviour, but also on the visual configuration with which the dynamics is associated.

Imagery of movements immediately following performance allows learning of motor skills that interfere.

Motor imagery, that is the mental rehearsal of a motor skill, can lead to improvements when performing the same skill. Here we show a powerful and complementary role, in which motor imagery of different movements after actually performing a skill allows learning that is not possible without imagery. We leverage a well-studied motor learning task in which subjects reach in the presence of a dynamic (force-field) perturbation. When two opposing perturbations are presented alternately for the same physical movement, there is substantial interference, preventing any learning. However, when the same physical movement is associated with follow-through movements that differ for each perturbation, both skills can be learned. Here we show that when subjects perform the skill and only imagine the follow-through, substantial learning occurs. In contrast, without such motor imagery there was no learning. Therefore, motor imagery can have a profound effect on skill acquisition even when the imagery is not of the skill itself. Our results suggest that motor imagery may evoke different neural states for the same physical state, thereby enhancing learning.

Motor Planning, Not Execution, Separates Motor Memories.

Recent theories of limb control emphasize motor cortex as a dynamical system, with planning setting the initial neural state, and execution arising from the self-limiting evolution of the intrinsic neural dynamics. Therefore, movements that share an initial trajectory but then diverge might have different neural states during the execution of the identical initial trajectories. We hypothesized that motor adaptation maps neural states to changes in motor command. This predicts that two opposing perturbations, which interfere when experienced over the same movement, could be learned if each is associated with a different plan even if not executed. We show that planning, but not executing, different follow-through movements allow opposing perturbations to be learned simultaneously over the same movement. However, no learning occurs if different follow throughs are executed, but not planned prior to movement initiation. Our results suggest neural, rather than physical states, are the critical factor associated with motor adaptation.