Figure 1 - uploaded by Alexander Rotenberg
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A drawing of a Necker cube. The Necker cube is an example of an ambiguous ¢gure that can be seen to jump between between two di¡erent states while continuously viewed.
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A key feature of perception is that the interpretation of a single, continuously available stimulus can change from time to time. This aspect of perception is well illustrated by the use of ambiguous figures that can be seen in two different ways. When people view such a stimulus they almost universally describe what they are seeing as jumping betw...
Citations
... The neural correlates underlying the organization of navigation behaviors has not received much attention. However, partial insight on this topic may be obtained from cue conflict experiments investigating the relative dominance of visual and self-motion cues on the firing properties of place cells (Rotenberg andMuller, 1997, Knierim et al., 1998) and/or head direction cells (Taube and Burton, 1995, Knierim et al., 1998, Zugaro et al., 2000 while rats forage for randomly scattered food rewards (see Etienne, 2003, for a review). While there are some disagreements between studies, they all observed that both cell types were predominantly controlled by visual cues in the case of little to no conflict. ...
... Conversely, for more severe conflicts (i.e., those that are introduced suddenly rather than gradually, or those that have a large disparity in the directive information), the firing of both place and head direction cells are typically less predictable. The most common response in this case is a shift in control to self-motion cues (Rotenberg andMuller, 1997, Knierim et al., 1998), although in at least one study head direction cells were observed to fire maximally in a direction intermediate between those corresponding to each cue type (Knierim et al., 1998, Fig. 2D). ...
Spatial navigation has received much attention from neuroscientists, leading to the identification of key brain areas and the discovery of numerous spatially selective cells. Despite this progress, our understanding of how the pieces fit together to drive behavior is generally lacking. We argue that this is partly caused by insufficient communication between behavioral and neuroscientific researchers. This has led the latter to under-appreciate the relevance and complexity of spatial behavior, and to focus too narrowly on characterizing neural representations of space-disconnected from the computations these representations are meant to enable. We therefore propose a taxonomy of navigation processes in mammals that can serve as a common framework for structuring and facilitating interdisciplinary research in the field. Using the taxonomy as a guide, we review behavioral and neural studies of spatial navigation. In doing so, we validate the taxonomy and showcase its usefulness in identifying potential issues with common experimental approaches, designing experiments that adequately target particular behaviors, correctly interpreting neural activity, and pointing to new avenues of research.
... The neural correlates underlying the organization of navigation behaviors has not received much attention. However, partial insight on this topic may be obtained from cue conflict experiments investigating the relative dominance of visual and self-motion cues on the firing properties of place cells (Rotenberg andMuller, 1997, Knierim et al., 1998) and/or head direction cells (Taube and Burton, 1995, Knierim et al., 1998, Zugaro et al., 2000 while rats forage for randomly scattered food rewards (see Etienne, 2003, for a review). While there are some disagreements between studies, they all observed that both cell types were predominantly controlled by visual cues in the case of little to no conflict. ...
... Conversely, for more severe conflicts (i.e., those that are introduced suddenly rather than gradually, or those that have a large disparity in the directive information), the firing of both place and head direction cells are typically less predictable. The most common response in this case is a shift in control to self-motion cues (Rotenberg andMuller, 1997, Knierim et al., 1998), although in at least one study head direction cells were observed to fire maximally in a direction intermediate between those corresponding to each cue type (Knierim et al., 1998, Fig. 2D). ...
An animal's ability to navigate space is crucial to its survival. It is also cognitively demanding, and relatively easy to probe. For these reasons, spatial navigation has received a great deal of attention from neuroscientists, leading to the identification of key brain areas and the ongoing discovery of a ``zoo'' of cell types responding to different aspects of spatial tasks. Despite this progress, our understanding of how the pieces fit together to drive behavior is generally lacking. We argue that this is partly caused by insufficient communication between researchers focusing on spatial behavior and those attempting to study its neural basis. This has led the latter to under-appreciate the relevance and complexity of spatial behavior, and to focus too narrowly on characterizing neural representations of space—disconnected from the computations these representations are meant to enable. We therefore propose a taxonomy of navigation processes in mammals that can serve as a common framework for structuring and facilitating interdisciplinary research in the field. Using the taxonomy as a guide, we review behavioral and neural studies of spatial navigation. In doing so, we both validate the taxonomy and showcase its usefulness in identifying potential issues with common experimental approaches, designing experiments that adequately target particular behaviors, correctly interpreting neural activity, and pointing to new avenues of research.
... Sometimes, the allocentric space perception may deviate far from the actual environment. Muller et al. changed the position of a visual cue on the wall in the presence of the rats and found that the place field was completely remapped when the cue had returned to its original position after an initial 180 rotation followed by four 45 rotations (Alexander and Muller 1997) (Fig. 7.5). In another experiment, O'Keefe and Speakman showed that the place firing pattern can be aligned only with the rat's choice of the goal arm, not the designated arm (O'Keefe and Speakman 1987), suggesting that the placespecific firing pattern reflects only what the animal gets. ...
... The two rows of place fields are results from two cells undergoing a series of visible cue card rotations. After combining visible 180 and 45 cue card rotation as illustrated from session 1 to session 6, the place field remaps into a new location within the identical environment (Alexander and Muller 1997) extend the current argument to path integration in other species, such as insects (Heinze et al. 2018;Pfeiffer and Homberg 2014). While birds are able to conduct path integration, and there are certain types of spatially specific firing patterns in the hippocampus (Mittelstaedt and Mittelstaedt 1982;Sherry et al. 2017), more experiments are needed to discuss this topic in birds. ...
Fear is defined as a fundamental emotion promptly arising in the context of threat and when danger is perceived. Fear can be innate or learned. Examples of innate fear include fears that are triggered by predators, pain, heights, rapidly approaching objects, and ancestral threats such as snakes and spiders. Animals and humans detect and respond more rapidly to threatening stimuli than to nonthreatening stimuli in the natural world. The threatening stimuli for most animals are predators, and most predators are themselves prey to other animals. Predatory avoidance is of crucial importance for survival of animals. Although humans are rarely affected by predators, we are constantly challenged by social threats such as a fearful or angry facial expression. This chapter will summarize the current knowledge on brain circuits processing innate fear responses to visual stimuli derived from studies conducted in mice and humans.
... Sometimes, the allocentric space perception may deviate far from the actual environment. Muller et al. changed the position of a visual cue on the wall in the presence of the rats and found that the place field was completely remapped when the cue had returned to its original position after an initial 180 rotation followed by four 45 rotations (Alexander and Muller 1997) (Fig. 7.5). In another experiment, O'Keefe and Speakman showed that the place firing pattern can be aligned only with the rat's choice of the goal arm, not the designated arm (O'Keefe and Speakman 1987), suggesting that the placespecific firing pattern reflects only what the animal gets. ...
... The two rows of place fields are results from two cells undergoing a series of visible cue card rotations. After combining visible 180 and 45 cue card rotation as illustrated from session 1 to session 6, the place field remaps into a new location within the identical environment (Alexander and Muller 1997) extend the current argument to path integration in other species, such as insects (Heinze et al. 2018;Pfeiffer and Homberg 2014). While birds are able to conduct path integration, and there are certain types of spatially specific firing patterns in the hippocampus (Mittelstaedt and Mittelstaedt 1982;Sherry et al. 2017), more experiments are needed to discuss this topic in birds. ...
In mammals, parental care is essential for the survival of the young; therefore, it is vitally important to the propagation of the species. These behaviors, differing between the two sexes, are innate, stereotyped, and are also modified by an individual’s reproductive experience. These characteristics suggest that neural mechanisms underlying parental behaviors are genetically hardwired, evolutionarily conserved as well as sexually differentiated and malleable to experiential changes. Classical lesion studies on neural control of parental behaviors, mostly done in rats, date back to the 1950s. Recent developments of new methods and tools in neuroscience, which allow precise targeting and activation/inhibition of specific populations of neurons and their projections to different brain structures, have afforded fresh opportunities to dissect and delineate the detailed neural circuit mechanisms that govern distinct components of parental behaviors in the genetically tractably organism, the laboratory mouse (Mus musculus). In this review, we summarize recent discoveries using modern neurobiological tools within the context of traditional lesion studies. In addition, we discuss interesting cross talk between neural circuits that govern parent care with those that regulate other innate behaviors such as feeding and mating.
... The most simple version of these experiments had a circular arena with a cue card on one side of the arena. The cue card could be rotated to any position in the arena, reported as an angle with respect to the original cue card orientation in the room reference frame (Rotenberg and Muller, 1997;Knierim et al., 1998;Hargreaves et al., 2007). Experiments reported two types of changes in place field behavior in response to a given manipulation. ...
... The animal is removed from the maze, which is cleaned and the cue card is rotated 180˚, before returning the animal. The finding is that place fields retain their positions relative to each other (no remapping) and relative to the card, so they rotate 180˚with respect to the room reference frame (offset of 180˚) (Rotenberg and Muller, 1997;Knierim et al., 1995). We model this by providing 10 single-dimensional training observations, each drawn from a wrapped normal with ¼ 0 ; s ¼ 18 , representing the position of the cue card. ...
... A similar experiment was performed where the cue card is rotated 180˚without removing the animal or cleaning the maze. The finding is that the place fields did not remap or rotate in response to this manipulation (Rotenberg and Muller, 1997). We model this with an expanded feature vector because the animal has access to additional cues, albeit cues that are less reliable than the cue card: namely, a preserved internal orientation from path integration and odor cues that the animal has left on the maze. ...
Cells in the hippocampus tuned to spatial location (place cells) typically change their tuning when an animal changes context, a phenomenon known as remapping. A fundamental challenge to understanding remapping is the fact that what counts as a ‘‘context change’’ has never been precisely defined. Furthermore, different remapping phenomena have been classified on the basis of how much the tuning changes after different types and degrees of context change, but the relationship between these variables is not clear. We address these ambiguities by formalizing remapping in terms of hidden state inference. According to this view, remapping does not directly reflect objective, observable properties of the environment, but rather subjective beliefs about the hidden state of the environment. We show how the hidden state framework can resolve a number of puzzles about the nature of remapping.
... The answer depends on the subject's prior experience with those cues. Distal cues are typically dominant (Kneirim and Hamilton, 2011;Yoganarasimha et al., 2006), but proximal and idiothetic, self-referring cues can dominate when visual cues are absent or experienced as unreliable (Chakraborty et al., 2004;Gupta et al., 2014;Jeffery, 1998;Jeffery and O'Keefe, 1999;Knierim et al., 1995;Mizumori and Williams, 1993;Rotenberg and Muller, 1997), and directional resetting can occur when orientation is journey dependent (Valerio and Taube, 2012). In the present experiment, the stationary and rotating sources of information remained useful and necessary Fenton and Bures, 2003) and encoded in MEC discharge (Figure 4), and hippocampal discharge and its utility for avoiding shock varied with the details of behavior (Kelemen and Fenton, 2010;van Dijk and Fenton, 2018). ...
Head-direction cells preferentially discharge when the head points in a particular azimuthal direction, are hypothesized to collectively function as a single neural system for a unitary direction sense, and are believed to be essential for navigating extra-personal space by functioning like a compass. We tested these ideas by recording medial entorhinal cortex (MEC) head-direction cells while rats navigated on a familiar, continuously rotating disk that dissociates the environment into two spatial frames: one stationary and one rotating. Head-direction cells degraded directional tuning referenced to either of the externally referenced spatial frames, but firing rates, sub-second cell-pair action potential discharge relationships, and internally referenced directional tuning were preserved. MEC head-direction cell ensemble discharge collectively generates a subjective, internally referenced unitary representation of direction that, unlike a compass, is inconsistently registered to external landmarks during navigation. These findings indicate that MEC-based directional information is subjectively anchored, potentially providing for navigation without a stable externally anchored direction sense.
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... The answer depends on the subject's prior experience with those cues. Distal cues are typically dominant (Kneirim and Hamilton, 2011;Yoganarasimha et al., 2006), but proximal and idiothetic, self-referring cues can dominate when visual cues are absent or experienced as unreliable (Chakraborty et al., 2004;Gupta et al., 2014;Jeffery, 1998;Jeffery and O'Keefe, 1999;Knierim et al., 1995;Mizumori and Williams, 1993;Rotenberg and Muller, 1997), and directional resetting can occur when orientation is journey dependent (Valerio and Taube, 2012). In the present experiment, the stationary and rotating sources of information remained useful and necessary Fenton and Bures, 2003) and encoded in MEC discharge (Figure 4), and hippocampal discharge and its utility for avoiding shock varied with the details of behavior (Kelemen and Fenton, 2010;van Dijk and Fenton, 2018). ...
Head-direction cells preferentially discharge when the head points in a particular azimuthal direction, are hypothesized to collectively function as a single neural system for a unitary direction sense, and are believed to be essential for navigating extra-personal space by functioning like a compass. We tested these ideas by recording medial entorhinal cortex (MEC) head-direction cells while rats navigated on a familiar, continuously rotating disk that dissociates the environment into two spatial frames: one stationary and one rotating. Head-direction cells degraded directional tuning referenced to either of the externally referenced spatial frames, but firing rates, sub-second cell-pair action potential discharge relationships, and internally referenced directional tuning were preserved. MEC head-direction cell ensemble discharge collectively generates a subjective, internally referenced unitary representation of direction that, unlike a compass, is inconsistently registered to external landmarks during navigation. These findings indicate that MEC-based directional information is subjectively anchored, potentially providing for navigation without a stable externally anchored direction sense.
... Their firing patterns are context-specific and reproducible under identical conditions after weeks and even months (Thompson and Best, 1990). External sensory cues provide a key stream of information for place cells, and their activity is acutely controlled by both visual cues (O'Keefe and Conway, 1978;Muller and Kubie, 1987;Rotenberg and Muller, 1997) as well as olfactory cues (Save et al., 2000;Anderson and Jeffery, 2003;Zhang and Manahan-Vaughan, 2015). Place cells also retain highly defined firing patterns in the absence of salient sensory cues (Quirk et al., 1990;Save et al., 2000;, which suggests that their activity is dependent on additional information derived from idiothetic cues (McNaughton et al., , 2006. ...
Spatial encoding in the hippocampus is based on a range of different input sources. To generate spatial representations, reliable sensory cues from the external environment are integrated with idiothetic cues, derived from self-movement, that enable path integration and directional perception. In this study, we examined to what extent idiothetic cues significantly contribute to spatial representations and navigation: we recorded place cells while rodents navigated towards two visually identical chambers in 180° orientation via two different paths in darkness and in the absence of reliable auditory or olfactory cues. Our goal was to generate a conflict between local visual and direction-specific information, and then to assess which strategy was prioritized in different learning phases. We observed that, in the absence of distal cues, place fields are initially controlled by local visual cues that override idiothetic cues, but that with multiple exposures to the paradigm, spaced at intervals of days, idiothetic cues become increasingly implemented in generating an accurate spatial representation. Taken together, these data support that, in the absence of distal cues, local visual cues are prioritized in the generation of context-specific spatial representations through place cells, whereby idiothetic cues are deemed unreliable. With cumulative exposures to the environments, the animal learns to attend to subtle idiothetic cues to resolve the conflict between visual and direction-specific information.
... First, it may solve major and sudden discrepancies in the hippocampal map orientation. A good example of this process is provided by the study of Rotenberg and Muller (1997). In this work, hippocampal place cells were recorded as a salient visual cue in the recording arena was rotated while the rat was in the apparatus. ...
... This manipulation puts into conflict visual stimuli (which indicate that the surroundings have moved) with self-motion stimuli (which indicate the surroundings are stable). Rotenberg and Muller (1997) found that if the card was rotated by a small angle (45 • ), fields almost always rotated equally whereas if the card was rotated by 180 • the fields almost always remained in their previous position. This effect is due to the conflict between external and self-motion cues. ...
Since the discovery of place cells, the hippocampus is thought to be the neural substrate of a cognitive map. The later discovery of head direction cells, grid cells and border cells, as well as of cells with more complex spatial signals, has led to the idea that there is a brain system devoted to providing the animal with the information required to achieve efficient navigation. Current questioning is focused on how these signals are integrated in the brain. In this review, we focus on the issue of how self-localization is performed in the hippocampal place cell map. To do so, we first shortly review the sensory information used by place cells and then explain how this sensory information can lead to two coding modes, respectively based on external landmarks (allothetic information) and self-motion cues (idiothetic information). We hypothesize that these two modes can be used concomitantly with the rat shifting from one mode to the other during its spatial displacements. We then speculate that sequential reactivation of place cells could participate in the resetting of self-localization under specific circumstances and in learning a new environment. Finally, we provide some predictions aimed at testing specific aspects of the proposed ideas.
... First, it may solve major and sudden discrepancies in the hippocampal map orientation. A good example of this process is provided by the study of Rotenberg and Muller (1997). In this work, hippocampal place cells were recorded as a salient visual cue in the recording arena was rotated while the rat was in the apparatus. ...
... This manipulation puts into conflict visual stimuli (which indicate that the surroundings have moved) with self-motion stimuli (which indicate the surroundings are stable). Rotenberg and Muller (1997) found that if the card was rotated by a small angle (45 • ), fields almost always rotated equally whereas if the card was rotated by 180 • the fields almost always remained in their previous position. This effect is due to the conflict between external and self-motion cues. ...
Since the discovery of place cells, the hippocampus is thought to be the neural substrate of a cognitive map. The later discovery of head direction cells, grid cells and border cells, as well as of cells with more complex spatial signals, has led to the idea that there is a brain system devoted to providing the animal with the information required to achieve efficient navigation. Current questioning is focused on how these signals are integrated in the brain. In this review, we focus on the issue of how self-localization is performed in the hippocampal place cell map. To do so, we first shortly review the sensory information used by place cells and then explain how this sensory information can lead to two coding modes, respectively based on external landmarks (allothetic information) and self-motion cues (idiothetic information). We hypothesize that these two modes can be used concomitantly with the rat shifting from one mode to the other during its spatial displacements. We then speculate that sequential reactivation of place cells could participate in the resetting of self-localization under specific circumstances and in learning a new environment. Finally, we provide some predictions aimed at testing specific aspects of the proposed ideas.
