The neural substrates of deliberative decision making: contrasting effects of hippocampus lesions on performance and vicarious trial-and-error behavior in a spatial memory task and a visual discrimination task

Vicarious trial-and-errors (VTEs) are back-and-forth movements of the head exhibited by rodents and other animals when faced with a decision. These behaviors have recently been associated with prospective sweeps of hippocampal place cell firing, and thus may reflect a rodent model of deliberative decision-making. The aim of the current study was to test whether the hippocampus is essential for VTEs in a spatial memory task and in a simple visual discrimination (VD) task. We found that lesions of the hippocampus with ibotenic acid produced a significant impairment in the accuracy of choices in a serial spatial reversal (SR) task. In terms of VTEs, whereas sham-lesioned animals engaged in more VTE behavior prior to identifying the location of the reward as opposed to repeated trials after it had been located, the lesioned animals failed to show this difference. In contrast, damage to the hippocampus had no effect on acquisition of a VD or on the VTEs seen in this task. For both lesion and sham-lesion animals, adding an additional choice to the VD increased the number of VTEs and decreased the accuracy of choices. Together, these results suggest that the hippocampus may be specifically involved in VTE behavior during spatial decision making

Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points

The hippocampus encodes both spatial and nonspatial aspects of a rat's ongoing behavior at the single-cell level. In this study, we examined the encoding of intended destination by hippocampal (CA1) place cells during performance of a serial reversal task on a double Y-maze. On the maze, rats had to make two choices to access one of four possible goal locations, two of which contained reward. Reward locations were kept constant within blocks of 10 trials but changed between blocks, and the session of each day comprised three or more trial blocks. A disproportionate number of place fields were observed in the start box and beginning stem of the maze, relative to other locations on the maze. Forty-six percent of these place fields had different firing rates on journeys to different goal boxes. Another group of cells had place fields before the second choice point, and, of these, 44% differentiated between journeys to specific goal boxes. In a second experiment, we observed that rats with hippocampal damage made significantly more errors than control rats on the Y-maze when reward locations were reversed. Together, these results suggest that, at the start of the maze, the hippocampus encodes both current location and the intended destination of the rat, and this encoding is necessary for the flexible response to changes in reinforcement contingencies

Navigation in Real-World Environments: New Opportunities Afforded by Advances in Mobile Brain Imaging

A central question in neuroscience and psychology is how the mammalian brain represents the outside world and enables interaction with it. Significant progress on this question has been made in the domain of spatial cognition, where a consistent network of brain regions that represent external space has been identified in both humans and rodents. In rodents, much of the work to date has been done in situations where the animal is free to move about naturally. By contrast, the majority of work carried out to date in humans is static, due to limitations imposed by traditional laboratory based imaging techniques. In recent years, significant progress has been made in bridging the gap between animal and human work by employing virtual reality (VR) technology to simulate aspects of real-world navigation. Despite this progress, the VR studies often fail to fully simulate important aspects of real-world navigation, where information derived from self-motion is integrated with representations of environmental features and task goals. In the current review article, we provide a brief overview of animal and human imaging work to date, focusing on commonalties and differences in findings across species. Following on from this we discuss VR studies of spatial cognition, outlining limitations and developments, before introducing mobile brain imaging techniques and describe technical challenges and solutions for real-world recording. Finally, we discuss how these advances in mobile brain imaging technology, provide an unprecedented opportunity to illuminate how the brain represents complex multifaceted information during naturalistic navigation

Navigation in real-world environments : new opportunities afforded by advances in mobile brain imaging

A central question in neuroscience and psychology is how the mammalian brain represents the outside world and enables interaction with it. Significant progress on this question has been made in the domain of spatial cognition, where a consistent network of brain regions that represent external space has been identified in both humans and rodents. In rodents, much of the work to date has been done in situations where the animal is free to move about naturally. By contrast, the majority of work carried out to date in humans is static, due to limitations imposed by traditional laboratory based imaging techniques. In recent years, significant progress has been made in bridging the gap between animal and human work by employing virtual reality (VR) technology to simulate aspects of real-world navigation. Despite this progress, the VR studies often fail to fully simulate important aspects of real-world navigation, where information derived from self-motion is integrated with representations of environmental features and task goals. In the current review article, we provide a brief overview of animal and human imaging work to date, focusing on commonalties and differences in findings across species. Following on from this we discuss VR studies of spatial cognition, outlining limitations and developments, before introducing mobile brain imaging techniques and describe technical challenges and solutions for real-world recording. Finally, we discuss how these advances in mobile brain imaging technology, provide an unprecedented opportunity to illuminate how the brain represents complex multifaceted information during naturalistic navigation.Publisher PDFPeer reviewe

Understanding minds in real-world environments : toward a mobile cognition approach

This work is supported by a scholarship from the University of Stirling and a research grant from SINAPSE (Scottish Imaging Network: A Platform for Scientific Excellence).There is a growing body of evidence that important aspects of human cognition have been marginalized, or overlooked, by traditional cognitive science. In particular, the use of laboratory-based experiments in which stimuli are artificial, and response options are fixed, inevitably results in findings that are less ecologically valid in relation to real-world behavior. In the present review we highlight the opportunities provided by a range of new mobile technologies that allow traditionally lab-bound measurements to now be collected during natural interactions with the world. We begin by outlining the theoretical support that mobile approaches receive from the development of embodied accounts of cognition, and we review the widening evidence that illustrates the importance of examining cognitive processes in their context. As we acknowledge, in practice, the development of mobile approaches brings with it fresh challenges, and will undoubtedly require innovation in paradigm design and analysis. If successful, however, the mobile cognition approach will offer novel insights in a range of areas, including understanding the cognitive processes underlying navigation through space and the role of attention during natural behavior. We argue that the development of real-world mobile cognition offers both increased ecological validity, and the opportunity to examine the interactions between perception, cognition and action—rather than examining each in isolation.Publisher PDFPeer reviewe

Mobile EEG identifies the re-allocation of attention during real-world activity

S.L., M.I. and D.I.D. are members of the SINAPSE collaboration (www.sinapse.ac.uk), a pooling initiative funded by the Scottish Funding Council and the Chief Scientific Office of the Scottish Executive.The distribution of attention between competing processing demands can have dramatic real-world consequences, however little is known about how limited attentional resources are distributed during real-world behaviour. Here we employ mobile EEG to characterise the allocation of attention across multiple sensory-cognitive processing demands during naturalistic movement. We used a neural marker of attention, the Event-Related Potential (ERP) P300 effect, to show that attention to targets is reduced when human participants walk compared to when they stand still. In a second experiment, we show that this reduction in attention is not caused by the act of walking per se. A third experiment identified the independent processing demands driving reduced attention to target stimuli during motion. ERP data reveals that the reduction in attention seen during walking reflects the linear and additive sum of the processing demands produced by visual and inertial stimulation. The mobile cognition approach used here shows how limited resources are precisely re-allocated according to the sensory processing demands that occur during real-world behaviour.Publisher PDFPeer reviewe

The medial entorhinal cortex is necessary for the stimulus control over hippocampal place fields by distal, but not proximal, landmarks

A fundamental property of place cells in the hippocampus is the anchoring of their firing fields to salient landmarks within the environment. However, it is unclear how such information reaches the hippocampus. In the current experiment, we tested the hypothesis that the stimulus control exerted by distal visual landmarks requires input from the medial entorhinal cortex (MEC). Place cells were recorded from mice with ibotenic acid lesions of the MEC (n = 7) and from sham-lesioned mice (n = 6) following 90° rotations of either distal landmarks or proximal cues in a cue- controlled environment. We found that lesions of the MEC impaired the anchoring of place fields to distal landmarks, but not proximal cues. We also observed that, relative to sham-lesioned mice, place cells in animals with MEC lesions exhibited significantly reduced spatial information and increased sparsity. These results support the view that distal landmark information reaches the hippocampus via the MEC, but that proximal cue information can do so via an alternative neural pathway

The head direction cell system and behavior:The effects of lesions to the lateral mammillary bodies on spatial memory in a novel landmark task and in the water maze

The head direction system is composed of neurons found in a number of connected brain areas that fire in a sharply tuned, directional way. The function of this system, however, has not been fully established. To assess this, we devised a novel spatial landmark task, comparable to the paradigms in which stimulus control has been assessed for spatially tuned neurons. The task took place in a large cylinder and required rats to dig in a specific sand cup, from among 16 alternatives, to obtain a food reward. The reinforced cup was in a fixed location relative to a salient landmark, and probe sessions confirmed that the landmark exerted stimulus control over the rats’ cup choices. To assess the contribution of the head direction cell system to this memory task, half of the animals received ibotenic acid infusions into the lateral mammillary nuclei (LMN), an essential node in the head direction network, while the other received sham lesions. No differences were observed in performance of this task between the 2 groups. Animals with LMN lesions were impaired, however, in reversal learning on a water maze task. These results suggest that the LMN, and potentially the head direction cell system, are not essential for the use of visual landmarks to guide spatial behavior

Field repetition and local mapping in the hippocampus and medial entorhinal cortex

Hippocampal place cells support spatial cognition and are thought to form the neural substrate of a global 'cognitive map'. A widely held view is that parts of the hippocampus also underlie the ability to separate patterns, or to provide different neural codes for distinct environments. However, a number of studies have shown that in environments composed of multiple, repeating compartments, place cells and other spatially modulated neurons show the same activity in each local area. This repetition of firing fields may reflect pattern completion, and may make it difficult for animals to distinguish similar local environments. In this review we will (a) highlight some of the navigation difficulties encountered by humans in repetitive environments, (b) summarise literature demonstrating that place and grid cells represent local and not global space, and (c) attempt to explain the origin of these phenomena. We argue that the repetition of firing fields can be a useful tool for understanding of the relationship between grid cells in the entorhinal cortex and place cells in the hippocampus, the spatial inputs shared by these cells, and the propagation of spatially-related signals through these structures

Place field repetition and spatial learning in a multicompartment environment

Recent studies have shown that place cells in the hippocampus possess firing fields that repeat in physically similar, parallel environments. These results imply that it should be difficult for animals to distinguish parallel environments at a behavioral level. To test this, we trained rats on a novel odor-location task in an environment with four parallel compartments which had previously been shown to yield place field repetition. A second group of animals was trained on the same task, but with the compartments arranged in different directions, an arrangement we hypothesised would yield less place field repetition. Learning of the odor-location task in the parallel compartments was significantly impaired relative to learning in the radially arranged compartments. Fewer animals acquired the full discrimination in the parallel compartments compared to those trained in the radial compartments, and the former also required many more sessions to reach criterion compared to the latter. To confirm that the arrangement of compartments yielded differences in place cell repetition, in a separate group of animals we recorded from CA1 place cells in both environments. We found that CA1 place cells exhibited repeated fields across four parallel local compartments, but did not do so when the same compartments were arranged radially. To confirm that the differences in place field repetition across the parallel and radial compartments depended on their angular arrangement, and not incidental differences in access to an extra-maze visual landmark, we repeated the recordings in a second set of rats in the absence of the orientation landmark. We found, once again, that place fields showed repetition in parallel compartments, and did not do so in radially arranged compartments. Thus place field repetition, or lack thereof, in these compartments was not dependent on extra-maze cues. Together, these results imply that place field repetition constrains spatial learning. © 2015 Wiley Periodicals, Inc