Attentive scanning behavior drives one-trial potentiation of hippocampal place fields

Rowland

Cold Spring Harb Perspect Biol

2015

407

267

The hippocampal system is critical for storage and retrieval of declarative memories, including memories for locations and events that take place at those locations. Spatial memories place high demands on capacity. Memories must be distinct to be recalled without interference and encoding must be fast. Recent studies have indicated that hippocampal networks allow for fast storage of large quantities of uncorrelated spatial information. The aim of the this article is to review and discuss some of this work, taking as a starting point the discovery of multiple functionally specialized cell types of the hippocampal-entorhinal circuit, such as place, grid, and border cells. We will show that grid cells provide the hippocampus with a metric, as well as a putative mechanism for decorrelation of representations, that the formation of environment-specific place maps depends on mechanisms for long-term plasticity in the hippocampus, and that long-term spatiotemporal memory storage may depend on offline consolidation processes related to sharp-wave ripple activity in the hippocampus. The multitude of representations generated through interactions between a variety of functionally specialized cell types in the entorhinal-hippocampal circuit may be at the heart of the mechanism for declarative memory formation.T he scientific study of human memory started with Herman Ebbinghaus, who initiated the quantitative investigation of associative memory processes as they take place (Ebbinghaus 1885). Ebbinghaus described the conditions that influence memory formation and he determined several basic principles of encoding and recall, such as the law of frequency and the effect of time on forgetting. With Ebbinghaus, higher mental functions were brought to the laboratory. In parallel with the human learning tradition that Ebbinghaus started, a new generation of experimental psychologists described the laws of associative learning in animals. With behaviorists like Pavlov, Watson, Hull, Skinner, and Tolman, a rigorous program for identifying the laws of animal learning was initiated. By the middle of the 20th century, a language for associative learning processes had been developed, and many of the fundamental relationships between environment and behavior had been described. What was completely missing, though, was an understanding of the neural activity underlying the formation of the memory. The behaviorists had deliberately shied away from physiological explanations because of the intangible nature of neural activity at that time.Then the climate began to change. Karl Lashley had shown that lesions in the cerebral cortex had predictable effects on behavior in Editors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at

Section: Memory Encodingsupporting

confidence: 70%

Section: Place Cells Synaptic Plasticity and Memorymentioning

confidence: 99%

Place Cells, Grid Cells, and Memory

Rowland

Cold Spring Harb Perspect Biol

2015

407

267

“…On one hand, scanning the possible routes to take allows acquiring sensory information regarding the environmental options. This increase in available sensory information could potentially increase the number of hippocampal place-cells tuned to the spatial locations of each of the maze-arms, as observed in 9 , thereby optimizing performance. On the other hand, aligning one's body towards possible decision options would allow the setting of path-integration hippocampal mechanisms to simulate future trajectories, as has been theoretically and computationally postulated 17,18 .…”

Section: Discussionmentioning

confidence: 99%

“…As expected, we have observed greater trajectory duration, length and IdPhi for the low-frequency condition when compared to the high-frequency condition, suggesting that frequency of exposure modulates the internal representation of the environment and/or experimental contingencies. Head-scanning behaviors have been observed to increase the activity of hippocampal place-cells leading to the potentiation of their receptive-fields at a given spatial location 9 . These results suggest one-trial encoding of experiences mediated by place-cell activity.…”

Section: Vte Decreases With Learningmentioning

confidence: 99%

“…However, the signatures of such learning/relearning and how experience affects them remain unclear. Head-scanning behaviors have been shown to relate to novelty detection and are suggested to serve the purpose of sensory acquisition 9 . Even though VTE has been mostly studied in rodents' spatial navigation, humans might also benefit from, and exhibit, such behavior.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Human vicarious trial and error is predictive of spatial navigation performance

Santos-Pata

Verschure

2018

Preprint

When learning new environments, rats often pause at decision points and look back and forth over their possible trajectories as if they were imagining the future outcome of their actions, a behavior termed "Vicarious trial and error" (VTE). As the animal learns the environmental configuration, rats change from deliberative to habitual behavior, and VTE tends to disappear, suggesting a functional relevance in the early stages of learning. Despite the extensive research on spatial navigation, learning and VTE in the rat model, fewer studies have focused on humans. Here, we tested whether head-scanning behaviors that humans typically exhibit during spatial navigation are as predictive of spatial learning as in the rat. Subjects performed a goal-oriented virtual navigation task in a symmetric environment. Spatial learning was assessed through the analysis of trajectories, timings, and head orientations, under habitual and deliberative spatial navigation conditions. As expected, we found that trajectory length and duration decreased with the trial number, implying that subjects learned the spatial configuration of the environment over trials. Interestingly, IdPhi (a standard metric of VTE) also decreased with the trial number, suggesting that humans benefit from the same head-orientation scanning behavior as rats at spatial decision-points. Moreover, IdPhi captured exclusively at the first decision-point of each trial, was correlated with trial trajectory duration and length. Our findings demonstrate that in VTE is a signature of the stage of spatial learning in humans, and can be used to predict performance in navigation tasks with high accuracy.

From the GPS to HM: Place cells, grid cells, and memory

Knierim

2015

Hippocampus

A longstanding debate in hippocampus research has revolved around how to reconcile spatial mapping functions of the hippocampus with the global amnesia produced by hippocampal damage in humans. Is the hippocampus primarily a cognitive map used to support spatial learning, or does it support more general types of learning necessary for declarative memory? In recent years, a general consensus has emerged that the hippocampus receives both spatial and nonspatial inputs from the entorhinal cortex. The hippocampus creates representations of experience in a particular spatial and temporal context. This process allows the individual components of experience to be stored in such a way that they can be retrieved together as a conscious recollection.