Neural codes for one’s own position and direction in a real-world “vista” environment

Humans, like animals, rely on an accurate knowledge of one’s spatial position and facing direction to keep orientated in the surrounding space. Although previous neuroimaging studies demonstrated that scene-selective regions (the parahippocampal place area or PPA, the occipital place area or OPA and the retrosplenial complex or RSC), and the hippocampus (HC) are implicated in coding position and facing direction within small-(room-sized) and large-scale navigational environments, little is known about how these regions represent these spatial quantities in a large open-field environment. Here, we used functional magnetic resonance imaging (fMRI) in humans to explore the neural codes of these navigationally-relevant information while participants viewed images which varied for position and facing direction within a familiar, real-world circular square. We observed neural adaptation for repeated directions in the HC, even if no navigational task was required. Further, we found that the amount of knowledge of the environment interacts with the PPA selectivity in encoding positions: individuals who needed more time to memorize positions in the square during a preliminary training task showed less neural attenuation in this scene-selective region. We also observed adaptation effects, which reflect the real distances between consecutive positions, in scene-selective regions but not in the HC. When examining the multi-voxel patterns of activity we observed that scene-responsive regions and the HC encoded both spatial information and that the RSC classification accuracy for positions was higher in individuals scoring higher to a self-reported questionnaire of spatial abilities. Our findings provide new insight into how the human brain represents a real, large-scale “vista” space, demonstrating the presence of neural codes for position and direction in both scene-selective and hippocampal regions, and revealing the existence, in the former regions, of a map-like spatial representation reflecting real-world distance between consecutive positions

Lifelong Learning of Spatiotemporal Representations with Dual-Memory Recurrent Self-Organization

Artificial autonomous agents and robots interacting in complex environments are required to continually acquire and fine-tune knowledge over sustained periods of time. The ability to learn from continuous streams of information is referred to as lifelong learning and represents a long-standing challenge for neural network models due to catastrophic forgetting. Computational models of lifelong learning typically alleviate catastrophic forgetting in experimental scenarios with given datasets of static images and limited complexity, thereby differing significantly from the conditions artificial agents are exposed to. In more natural settings, sequential information may become progressively available over time and access to previous experience may be restricted. In this paper, we propose a dual-memory self-organizing architecture for lifelong learning scenarios. The architecture comprises two growing recurrent networks with the complementary tasks of learning object instances (episodic memory) and categories (semantic memory). Both growing networks can expand in response to novel sensory experience: the episodic memory learns fine-grained spatiotemporal representations of object instances in an unsupervised fashion while the semantic memory uses task-relevant signals to regulate structural plasticity levels and develop more compact representations from episodic experience. For the consolidation of knowledge in the absence of external sensory input, the episodic memory periodically replays trajectories of neural reactivations. We evaluate the proposed model on the CORe50 benchmark dataset for continuous object recognition, showing that we significantly outperform current methods of lifelong learning in three different incremental learning scenario

Grid Cell Hexagonal Patterns Formed by Fast Self-Organized Learning within Entorhinal Cortex

Grid cells in the dorsal segment of the medial entorhinal cortex (dMEC) show remarkable hexagonal activity patterns, at multiple spatial scales, during spatial navigation. How these hexagonal patterns arise has excited intense interest. It has previously been shown how a selforganizing map can convert firing patterns across entorhinal grid cells into hippocampal place cells that are capable of representing much larger spatial scales. Can grid cell firing fields also arise during navigation through learning within a self-organizing map? A neural model is proposed that converts path integration signals into hexagonal grid cell patterns of multiple scales. This GRID model creates only grid cell patterns with the observed hexagonal structure, predicts how these hexagonal patterns can be learned from experience, and can process biologically plausible neural input and output signals during navigation. These results support a unified computational framework for explaining how entorhinal-hippocampal interactions support spatial navigation.CELEST, a National Science Foundation Science of Learning Center (SBE-0354378); SyNAPSE program of Defense Advanced Research Projects Agency (HR00ll-09-3-0001, HR0011-09-C-0011

Integrating Spatial Working Memory and Remote Memory: Interactions between the Medial Prefrontal Cortex and Hippocampus

In recent years, two separate research streams have focused on information sharing between the medial prefrontal cortex (mPFC) and hippocampus (HC). Research into spatial working memory has shown that successful execution of many types of behaviors requires synchronous activity in the theta range between the mPFC and HC, whereas studies of memory consolidation have shown that shifts in area dependency may be temporally modulated. While the nature of information that is being communicated is still unclear, spatial working memory and remote memory recall is reliant on interactions between these two areas. This review will present recent evidence that shows that these two processes are not as separate as they first appeared. We will also present a novel conceptualization of the nature of the medial prefrontal representation and how this might help explain this area’s role in spatial working memory and remote memory recall

Slowness and Sparseness Lead to Place, Head-Direction, and Spatial-View Cells

We present a model for the self-organized formation of place cells, head-direction cells, and spatial-view cells in the hippocampal formation based on unsupervised learning on quasi-natural visual stimuli. The model comprises a hierarchy of Slow Feature Analysis (SFA) nodes, which were recently shown to reproduce many properties of complex cells in the early visual system. The system extracts a distributed grid-like representation of position and orientation, which is transcoded into a localized place-field, head-direction, or view representation, by sparse coding. The type of cells that develops depends solely on the relevant input statistics, i.e., the movement pattern of the simulated animal. The numerical simulations are complemented by a mathematical analysis that allows us to accurately predict the output of the top SFA laye

Beta Oscillations and Hippocampal Place Cell Learning during Exploration of Novel Environments

Berke et al. (2008) reported that beta oscillations occur during the learning of hippocampal place cell receptive fields in novel environments. Place cell selectivity can develop within seconds to minutes, and can remain stable for months. Paradoxically, beta power was very low during the first lap of exploration, grew to full strength as a mouse traversed a lap for the second and third times, and became and remained low again after the first two minutes of exploration. Beta oscillation power also correlated with the rate at which place cells became spatially selective, and not with theta oscillations. We explain such beta oscillations as a consequence of how place cell receptive fields may be learned as spatially selective categories due to feedback interactions between entorhinal cortex and hippocampus. Top-down attentive feedback helps to ensure rapid learning and stable memory of place cells. Beta oscillations are generated when top-down feedback mismatches bottom-up data as place cell receptive fields are refined. Beta oscillations do not occur on the first trial because adaptive weights in feedback pathways are all sufficiently large then to match any input pattern. On subsequent trials, adaptive weights become pruned as they learn to match the sharpening receptive fields of the place cell categories, thereby causing mismatches until place cell receptive fields stabilize.National Science Foundation (SBE-0354378

The hippocampus and cerebellum in adaptively timed learning, recognition, and movement

The concepts of declarative memory and procedural memory have been used to distinguish two basic types of learning. A neural network model suggests how such memory processes work together as recognition learning, reinforcement learning, and sensory-motor learning take place during adaptive behaviors. To coordinate these processes, the hippocampal formation and cerebellum each contain circuits that learn to adaptively time their outputs. Within the model, hippocampal timing helps to maintain attention on motivationally salient goal objects during variable task-related delays, and cerebellar timing controls the release of conditioned responses. This property is part of the model's description of how cognitive-emotional interactions focus attention on motivationally valued cues, and how this process breaks down due to hippocampal ablation. The model suggests that the hippocampal mechanisms that help to rapidly draw attention to salient cues could prematurely release motor commands were not the release of these commands adaptively timed by the cerebellum. The model hippocampal system modulates cortical recognition learning without actually encoding the representational information that the cortex encodes. These properties avoid the difficulties faced by several models that propose a direct hippocampal role in recognition learning. Learning within the model hippocampal system controls adaptive timing and spatial orientation. Model properties hereby clarify how hippocampal ablations cause amnesic symptoms and difficulties with tasks which combine task delays, novelty detection, and attention towards goal objects amid distractions. When these model recognition, reinforcement, sensory-motor, and timing processes work together, they suggest how the brain can accomplish conditioning of multiple sensory events to delayed rewards, as during serial compound conditioning.Air Force Office of Scientific Research (F49620-92-J-0225, F49620-86-C-0037, 90-0128); Advanced Research Projects Agency (ONR N00014-92-J-4015); Office of Naval Research (N00014-91-J-4100, N00014-92-J-1309, N00014-92-J-1904); National Institute of Mental Health (MH-42900