Place Cells, Head Direction Cells, and the Learning of Landmark Stability
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Activity Strength Within Optic Flow-Sensitive Cortical Regions Is Associated with Visual Path Integration Accuracy in Aged Adults
brain sciences Article Activity Strength within Optic Flow-Sensitive Cortical Regions Is Associated with Visual Path Integration Accuracy in Aged Adults Lauren Zajac 1,2,* and Ronald Killiany 1,2 1 Department of Anatomy & Neurobiology, Boston University School of Medicine, 72 East Concord Street (L 1004), Boston, MA 02118, USA; [email protected] 2 Center for Biomedical Imaging, Boston University School of Medicine, 650 Albany Street, Boston, MA 02118, USA * Correspondence: [email protected] Abstract: Spatial navigation is a cognitive skill fundamental to successful interaction with our envi- ronment, and aging is associated with weaknesses in this skill. Identifying mechanisms underlying individual differences in navigation ability in aged adults is important to understanding these age- related weaknesses. One understudied factor involved in spatial navigation is self-motion perception. Important to self-motion perception is optic flow–the global pattern of visual motion experienced while moving through our environment. A set of optic flow-sensitive (OF-sensitive) cortical regions was defined in a group of young (n = 29) and aged (n = 22) adults. Brain activity was measured in this set of OF-sensitive regions and control regions using functional magnetic resonance imaging while participants performed visual path integration (VPI) and turn counting (TC) tasks. Aged adults had stronger activity in RMT+ during both tasks compared to young adults. Stronger activity in the OF-sensitive regions LMT+ and RpVIP during VPI, not TC, was associated with greater VPI Citation: Zajac, L.; Killiany, R. accuracy in aged adults. The activity strength in these two OF-sensitive regions measured during Activity Strength within Optic VPI explained 42% of the variance in VPI task performance in aged adults. -
Position–Theta-Phase Model of Hippocampal Place Cell Activity Applied to Quantification of Running Speed Modulation of Firing Rate
Position–theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate Kathryn McClaina,b,1, David Tingleyb, David J. Heegera,c,1, and György Buzsákia,b,1 aCenter for Neural Science, New York University, New York, NY 10003; bNeuroscience Institute, New York University, New York, NY 10016; and cDepartment of Psychology, New York University, New York, NY 10003 Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved November 18, 2019 (received for review July 24, 2019) Spiking activity of place cells in the hippocampus encodes the Another challenge in understanding this system is the dynamic animal’s position as it moves through an environment. Within a interaction between the rate code and phase code. As these codes cell’s place field, both the firing rate and the phase of spiking in combine, different formats of information are conveyed simulta- the local theta oscillation contain spatial information. We propose a neously in place cell spiking. The interaction can produce unin- – position theta-phase (PTP) model that captures the simultaneous tuitive, although entirely predictable, results in traditional analyses expression of the firing-rate code and theta-phase code in place cell of place cell activity. These practical challenges have hindered the spiking. This model parametrically characterizes place fields to com- pare across cells, time, and conditions; generates realistic place cell effort to explain variability in hippocampal firing rates. A com- simulation data; and conceptualizes a framework for principled hy- putational tool is needed that accounts for the well-established pothesis testing to identify additional features of place cell activity. -
Beta Oscillations and Hippocampal Place Cell Learning During
Beta Oscillations and Hippocampal Place Cell Learning during Exploration of Novel Environments Stephen Grossberg1 1Department of Cognitive and Neural Systems Center for Adaptive Systems, and Center of Excellence for Learning in Education, Science and Technology Boston University 677 Beacon St Boston, Massachusetts 02215 [email protected] Telephone: 617-353-7858/7 Fax: 617-353-7755 http://www.cns.bu.edu/~steve July 29, 2008 Revised: November 24, 2008 CAS/CNS-TR-08-003 Hippocampus, in press Running head: Beta Oscillations during Hippocampal Place Cell Learning Corresponding author: Stephen Grossberg, [email protected] Keywords: grid cells, category learning, spatial navigation, adaptive resonance theory, entorhinal cortex 1 Abstract The functional role of synchronous oscillations in various brain processes has attracted a lot of experimental interest. Berke et al. (2008) reported beta oscillations during the learning of hippocampal place cell receptive fields in novel environments. Such 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 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. These beta oscillation properties are explained by a neural model of how place cell receptive fields may be learned and stably remembered as spatially selective categories due to feedback interactions between entorhinal cortex and hippocampus. This explanation allows the learning of place cell receptive fields to be understood as a variation of category learning processes that take place in many brain systems, and challenges hippocampal models in which beta oscillations and place cell stability cannot be explained. -
Representation of Spatial Orientation by the Intrinsic Dynamics of the Head-Direction Cell Ensemble: a Theory
The Journal of Neuroscience, March 15, 1996, 16(6):2112-2126 Representation of Spatial Orientation by the Intrinsic Dynamics of the Head-Direction Cell Ensemble: A Theory Kechen Zhang Department of Cognitive Science, University of California at San Diego, La Jolla, California 92093-05 15 The head-direction (HD) cells found in the limbic system in disturbances to its shape, and the shift speed can be controlled freely moving rats represent the instantaneous head direction accurately by the strength of the odd-weight component. The of the animal in the horizontal plane regardless of the location generic formulation of the shift mechanism is determined of the animal. The internal direction represented by these cells uniquely within the current theoretical framework. The attractor uses both self-motion information for inet-tially based updating dynamics of the system ensures modality-independence of the and familiar visual landmarks for calibration. Here, a model of internal representation and facilitates the correction for cumu- the dynamics of the HD cell ensemble is presented. The sta- lative error by the putative local-view detectors. The model bility of a localized static activity profile in the network and a offers a specific one-dimensional example of a computational dynamic shift mechanism are explained naturally by synaptic mechanism in which a truly world-centered representation can weight distribution components with even and odd symmetry, be derived from observer-centered sensory inputs by integrat- respectively. Under symmetric weights or symmetric reciprocal ing self-motion information. connections, a stable activity profile close to the known direc- Key words: head-direction cell; spatial orientation; attractor tional tuning curves will emerge. -
The Brain Compass: a Perspective on How Self-Motion Updates the Head Direction Cell Attractor
bioRxiv preprint doi: https://doi.org/10.1101/189464; this version posted September 17, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. The brain compass: a perspective on how self-motion updates the head direction cell attractor Jean Laurens, Dora E. Angelaki Dept. of Neuroscience, Baylor College of Medicine, Houston, TX, 77030, USA This study was supported by National Institutes of Health grants R21 NS098146 and R01- DC004260. Address for correspondence: Angelaki, Dora Department of Neuroscience Baylor College of Medicine One Baylor Plaza Houston, TX 77030 Office: (713) 798-1469 E-mail: [email protected] ABSTRACT Head Direction cells form an internal compass that signals head azimuth orientation even in the absence of visual landmarks. It is well accepted that head direction properties are generated through a ring attractor that is updated using rotation self-motion cues. The properties and origin of this self-motion velocity drive remain, however, unknown. We propose a unified, quantitative framework whereby the attractor velocity input represents a multisensory self-motion estimate computed through an internal model that uses sensory prediction error based on vestibular, visual, and somatosensory cues to improve on-line motor drive. We show how context- dependent strength of recurrent connections within the attractor itself, rather than the self- motion input, explain differences in head direction cell firing between free foraging and restrained movements. We also summarize recent findings on how head tilt relative to gravity influences the azimuth coding of head direction cells, and explain why and how these effects reflect an updating self-motion velocity drive that is not purely egocentric. -
Head Direction Cells: Properties and Functional Significance Robert U Mullet-L, James B Ranck Jr* and Jeffrey S Taubea
196 Head direction cells: properties and functional significance Robert U Mullet-l, James B Ranck Jr* and Jeffrey S Taubea The strong signal carried by head direction cells in the Under all known circumstances, postsubicular HD cells, postsubiculum complements the positional signal carried the first class to be discovered, discharge only as a by hippocampal place cells; together, the directional and function of the direction in which the rat’s head points positional signals provide the information necessary to permit in the horizontal plane, independent of head location. rats to generate and carry out intelligent, efficient solutions Postsubicular HD cell discharge is rapid only when the to spatial problems. Our opinion is that the hippocampal head points in an -90” sector of headings centered on a positional system acts as a cognitive map and that the role ‘preferred direction’. The relationship between direction of the directional system is to put the map into register with and discharge rate is steep; the function is triangular, the environment. In this way, paths found using the map can so that firing rate decreases linearly in both directions be properly executed. Head direction cells have recently been away from the preferred direction, to be nearly zero when discovered in parts of the thalamus reciprocally connected 45” away from the peak [2,3’]. In contrast to place cells, with the postsubiculum; such cells provide important clues to the reliability of postsubicular HD cell firing is very the organization of the directional system. high. (Some of the properties of HD cells are shown in Figure 2c.) Addresses tg2Department of Physiology, SUNY Health Science Center at In this review, we will first briefly recapitulate what is Brooklyn, 450 Clarkson Avenue, Brooklyn, New York 11203, USA known about HD cells (also called directional cells), t e-mail: [email protected] and then summarize what has been learned about them se-mail: [email protected] during the past two years. -
Behavioral Strategies, Sensory Cues, and Brain Mechanisms
Intro to Neuroscience: Behavioral Neuroscience Animal Navigation: Behavioral strategies, sensory cues, and brain mechanisms Nachum Ulanovsky Department of Neurobiology, Weizmann Institute of Science Outline of today’s lecture • Introduction: Feats of animal navigation • Navigational strategies: • Beaconing • Route following • Path integration • Map and Compass / Cognitive Map • Sensory cues for navigation: • Compass mechanisms • Map mechanisms • Brain mechanisms of Navigation (brief introduction) • Summary Outline of today’s lecture • Introduction: Feats of animal navigation • Navigational strategies: • Beaconing • Route following • Path integration • Map and Compass / Cognitive Map • Sensory cues for navigation: • Compass mechanisms • Map mechanisms • Brain mechanisms of Navigation (brief introduction) • Summary Shearwater migration across the pacific יסעור Population data from 19 birds 3 pairs of birds Recaptured at their breeding Shaffer et al. PNAS 103:12799-12802 (2006) grounds in New Zealand Some other famous examples • Wandering Albatross: finding a tiny island in the vast ocean • Salmon: returning to the river of birth after years in the ocean • Sea Turtles • Monarch Butterflies • Spiny Lobsters • … And many other examples (some of them we will see later) Mammals can also do it… Medium-scale navigation: Egyptian fruit bats navigating to an individual tree Tsoar, Nathan, Bartan, Vyssotski, Dell’Omo & Ulanovsky (PNAS, 2011) GPS movie: Bat 079 A typical example of a full night flight of an individual bat released @ cave Bat roost Foraging tree 5 Km Characteristics of the bats’ commuting flights: • Long-distance flights (often > 15 km one-way) • Very straight flights (straightness index > 0.9 for almost all bats) • Very fast (typically 30–40 km/hr, and up to 63 km/hr) • Very high (typically 100–200 meters, and up to 643 m) • Bats returned to the same individual tree night after night, for many nights tree cave Tsoar, Nathan, Bartan, With Vyssotski, Dell’Omo & Y. -
Spatial Linear Navigation: Is Vision Necessary? Isabelle Israël, Aurore Capelli, Anne-Emmanuelle Priot, I
Spatial linear navigation: Is vision necessary? Isabelle Israël, Aurore Capelli, Anne-Emmanuelle Priot, I. Giannopulu To cite this version: Isabelle Israël, Aurore Capelli, Anne-Emmanuelle Priot, I. Giannopulu. Spatial linear navigation: Is vision necessary?. Neuroscience Letters, Elsevier, 2013, 554, pp.34-38. 10.1016/j.neulet.2013.08.060. hal-02395669 HAL Id: hal-02395669 https://hal.archives-ouvertes.fr/hal-02395669 Submitted on 5 Dec 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Elsevier Editorial System(tm) for Neuroscience Letters Manuscript Draft Manuscript Number: Title: Spatial linear navigation : is vision necessary ? Article Type: Research Paper Keywords: Path integration; self-motion perception; multisensory integration Corresponding Author: Dr. Isabelle Israel, PhD Corresponding Author's Institution: CNRS First Author: Isabelle ISRAEL, PhD Order of Authors: Isabelle ISRAEL, PhD; Aurore CAPELLI, PhD; Anne-Emmanuelle PRIOT, MD, PhD; Irini GIANNOPULU, PhD, D.Sc. Abstract: In order to analyze spatial linear navigation through a task of self-controlled reproduction, healthy participants were passively transported on a mobile robot at constant velocity, and then had to reproduce the imposed distance of 2 to 8 m in two conditions: "with vision" and "without vision". -
Path Integration Deficits During Linear Locomotion After Human Medial Temporal Lobectomy
Path Integration Deficits during Linear Locomotion after Human Medial Temporal Lobectomy John W.Philbeck 1,Marlene Behrmann 2,Lucien Levy 3, Samuel J.Potolicchio 3,andAnthony J.Caputy 3 Abstract & Animalnavigation studies have implicated structures inand both adecrease inthe consistency ofpath integration and a around the hippocampal formation as crucialin performing systematic underregistration oflinear displacement (and/or path integration (amethod ofdetermining one’s position by velocity) during walking.Moreover, the deficits were observable monitoring internally generated self-motion signals). Less is even when there were virtually no angular acceleration known about the role ofthese structures forhuman path vestibular signals. Theresults suggest that structures inthe integration. We tested path integration inpatients whohad medial temporal lobe participate inhuman path integration undergone left orright medial temporal lobectomy as therapy when individuals walkalong linearpaths and that thisis so to forepilepsy. Thisprocedure removed approximately 50% ofthe agreater extent inright hemisphere structures than left. anterior portion ofthe hippocampus, as wellas the amygdala Thisinformation is relevant forfuture research investigating and lateral temporal lobe. Participants attempted to walk the neural substrates ofnavigation, not only inhumans without vision to apreviously viewed target 2–6 mdistant. (e.g.,functional neuroimaging and neuropsychological studies), Patients withright, but not left,hemisphere lesions exhibited but also -
Path Integration in Place Cells of Developing Rats PNAS PLUS
Path integration in place cells of developing rats PNAS PLUS Tale L. Bjerknesa,b, Nenitha C. Dagslotta,b, Edvard I. Mosera,b, and May-Britt Mosera,b,1 aKavli Institute for Systems Neuroscience, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway; and bCentre for Neural Computation, Norwegian University of Science and Technology, NO-7489 Trondheim, Norway Contributed by May-Britt Moser, January 2, 2018 (sent for review November 1, 2017; reviewed by John L. Kubie and Mayank R. Mehta) Place cells in the hippocampus and grid cells in the medial entorhinal Firing locations of grid cells and place cells are not determined cortex rely on self-motion information and path integration for exclusively by path integration, however. Position information may spatially confined firing. Place cells can be observed in young rats be obtained also from distal landmarks, as suggested by the fact that as soon as they leave their nest at around 2.5 wk of postnatal life. In place fields (17) as well as grid fields (18, 19) follow the location of contrast, the regularly spaced firing of grid cells develops only after the walls of the recording environment when the environment is weaning, during the fourth week. In the present study, we sought to stretched or compressed. This observation points to local bound- determine whether place cells areabletointegrateself-motion aries as a strong determinant of firing location. On the other hand, information before maturation of the grid-cell system. Place cells other work has demonstrated that place cells fire in a predictable were recorded on a 200-cm linear track while preweaning, post- relationship to the animal’s start location on a linear track even weaning, and adult rats ran on successive trials from a start wall to a when the position of the starting point is shifted (20, 21). -
May-Britt Moser Norwegian University of Science and Technology (NTNU), Trondheim, Norway
Grid Cells, Place Cells and Memory Nobel Lecture, 7 December 2014 by May-Britt Moser Norwegian University of Science and Technology (NTNU), Trondheim, Norway. n 7 December 2014 I gave the most prestigious lecture I have given in O my life—the Nobel Prize Lecture in Medicine or Physiology. Afer lectures by my former mentor John O’Keefe and my close colleague of more than 30 years, Edvard Moser, the audience was still completely engaged, wonderful and responsive. I was so excited to walk out on the stage, and proud to present new and exciting data from our lab. Te title of my talk was: “Grid cells, place cells and memory.” Te long-term vision of my lab is to understand how higher cognitive func- tions are generated by neural activity. At frst glance, this seems like an over- ambitious goal. President Barack Obama expressed our current lack of knowl- edge about the workings of the brain when he announced the Brain Initiative last year. He said: “As humans, we can identify galaxies light years away; we can study particles smaller than an atom. But we still haven’t unlocked the mystery of the three pounds of matter that sits between our ears.” Will these mysteries remain secrets forever, or can we unlock them? What did Obama say when he was elected President? “Yes, we can!” To illustrate that the impossible is possible, I started my lecture by showing a movie with a cute mouse that struggled to bring a biscuit over an edge and home to its nest. Te biscuit was almost bigger than the mouse itself. -
Visual Influence on Path Integration in Darkness Indicates a Multimodal Representation of Large-Scale Space
Visual influence on path integration in darkness indicates a multimodal representation of large-scale space Lili Tcheanga,b,1, Heinrich H. Bülthoffb,d,1, and Neil Burgessa,c,1 aUCL Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom; bMax Planck Institute for Biological Cybernetics, Tuebingen 72076, Germany; cUCL Institute of Neurology, University College London, London WC1N 3BG, United Kingdom; and dDepartment of Brain and Cognitive Engineering, Korea University, Seoul 136-713, Korea Edited by Charles R. Gallistel, Rutgers University, Piscataway, NJ, and approved November 11, 2010 (received for review August 10, 2010) Our ability to return to the start of a route recently performed in representations are sufficiently abstract to support other actions darkness is thought to reflect path integration of motion-related in- aimed at the target location, such as throwing (19). formation. Here we provide evidence that motion-related interocep- To specifically examine the relationship between visual and in- tive representations (proprioceptive, vestibular, and motor efference teroceptive inputs to navigation, we investigated the effect of ma- copy) combine with visual representations to form a single multi- nipulating visual information. In the first experiment, we investigated modal representation guiding navigation. We used immersive virtual whether visual information present during the outbound trajectory reality to decouple visual input from motion-related interoception by makes an important contribution