Space in the brain: cells, circuits, codes and cognition
A theme issue of Philosophical Transactions of the Royal Society B based on a Theo Murphy Meeting held at The Royal Society at Chicheley Hall, home of the Kavli Royal Society International Centre, Buckinghamshire on 01-03 May 2013.
Edited by Tom Hartley, Colin Lever, Neil Burgess and John O’Keefe
February 05 2014; 369 (1635)
Online date: 23rd December 2013 http://rstb.royalsocietypublishing.org/site/2014/space.xhtml
Contact: Tom Hartley – [email protected]
How do we know where we are? How do we find our way? Why do we sometimes get lost? Neuroscientific research has revealed brain cells in the hippocampal formation that provide an exquisite representation of an animal or human being’s current location and heading. This “cognitive map” allows us to find our way around and provides the basis for lasting memories. This Theme Issue illustrates this exceptionally integrative branch of neuroscience, in which we join the dots, from molecules to cells, to complex behaviour and human cognition. It brings together the world leading experts in this area to integrate advances in optogenetics, virtual-reality, inducible transgenics, neuroimaging and computational neuroscience to define the neural mechanisms of navigation, with implications extending to behavioural genetics, robotics and medicine.
This issue is based on a Theo Murphy international scientific meeting held at The Royal Society at Chicheley Hall, home of the Kavli Royal Society International Centre, Buckinghamshire on 01-03 May 2013. More information and the speaker list can be found at http://royalsociety.org/events/2013/brain-circuits-cognition/
Dedication: Robert U. Muller (1942–2013) URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0618 by O’Keefe, John
Introduction: Space in the brain: how the hippocampal formation supports spatial cognition URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0510 by Hartley, Tom; Lever, Colin; Burgess, Neil; O'Keefe, John
Introduces a special issue on "Space in the Brain". How do we know where we are? How do we find our way? Why do we sometimes get lost? Neuroscientific research has revealed brain cells in the hippocampal formation that provide an exquisite representation of an animal or human being’s current location and heading. This “cognitive map” allows us to find our way around and provides the basis for lasting memories. We review the very latest findings which illustrate an exceptionally integrative branch of neuroscience in which we join the dots, from molecules to cells, to complex behaviour and human cognition. Contact: Dr Tom Hartley, University of York, [email protected], 441904322903
Architecture of spatial circuits in the hippocampal region URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0515 by Witter, Menno; Canto, Cathrin; Couey, Jonathan; Koganezawa, Noriko; O'Reilly, Kally
The hippocampal region is a part of the brain that is crucially involved in memory processes, including those used to navigate in space. The hippocampal region contains several neuron types that show distinct spatial firing patterns. The region is also known for its diversity in neural circuits and many have attempted to causally relate network architecture to functional outcome. In this review the architecture of local networks will be explored and we will describe how they may interact within the context of an overarching navigation circuit, aiming to provide directions for future research. Contact: Prof. Menno Witter, NTNU, [email protected], +47 73598249
Functional connectivity of the entorhinal-hippocampal space circuit URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0516 [OPEN ACCESS] by Zhang, Sheng-Jia; Ye, Jing; Couey, Jonathan; Witter, Menno; Moser, Edvard; Moser, May-Britt
The mammalian space circuit is known to contain several functionally specialized cell types, such as place cells in the hippocampus and grid cells, head-direction cells and border cells in the medial entorhinal cortex (MEC). The interaction between the entorhinal and hippocampal spatial representations is poorly understood, however. The present paper shows how new transgenic methods can be used to determine how cell types of the MEC are connected to place cells of the hippocampus. Contact: Prof. May-Britt Moser, Norwegian University of Science and Technology, [email protected], 73598277
The development of spatial behaviour and the hippocampal neural representation of space URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0409 [OPEN ACCESS] by Wills, Thomas; Muessig, Laurenz; Cacucci, Francesca
The hippocampus (a brain structure buried within our temporal lobes) is important for remembering places and founding our way around. A long tradition of research has uncovered the neural underpinnings of its cognitive function: neurons that encode the organism’s position, direction and distance travelled. More recently, researchers have started to address the question of how and when these spatial neural maps are built during the development of the brain. These studies promise to answer the long standing question of whether spatial concepts are learnt through experiencing spatial relations or whether each organism inherits them for free, through its evolutionary history. Contact: Dr Thomas Wills, University College London, [email protected]
Functional correlates of the lateral and medial entorhinal cortex: objects, path integration, and local-global reference frames URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0369 by Knierim, James; Neunuebel, Joshua; Deshmukh, Sachin
Our memories of our past experiences rely on a brain region called the hippocampus. This region is thought to combine a signal about "where we were" with a signal about "what happened there" in order to lay down the memory in a way that it can be later recalled as a conscious recollection. We identify these two components of memory with the two brain regions that provide the major input to the hippocampus. Contact: Dr James Knierim, Johns Hopkins University, [email protected]
Independence of landmark and self-motion guided navigation: a different role for grid cells URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0370 by Poucet, Bruno; Sargolini, Francesca; Song, Eun; Hangya, Balazs; Fox, Steven; Muller, Robert U. Note: Robert U. Muller died in September 2013.
We present a modified theory of navigation by rodents in which information obtained from landmarks is processed independently of information obtained from the animal’s self-motion. In this theory, “grid cells” (characterized by regular arrays of active regions) are updated from place cells in the light. Conversely, in the dark, grid cells are driven by self-motion cues and are used in lieu of landmark signals to help estimate the animal’s location. Intuitively, in the dark, the grid cells allow the animal and its place cells to calculate what it should be seeing, given the best available guess of its location. Contact: Dr Steven Fox, SUNY Downstate, [email protected]
Weighted cue integration in the rodent head direction system URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0512 [OPEN ACCESS] by Knight, Rebecca; Piette, Caitlin; Page, Hector; Walters, Daniel; Marozzi, Elizabeth; Nardini, Marko; Stringer, Simon; Jeffery, Kathryn
How does an animal know which way it is facing? Here, we show that the brain finds a compromise between its previous internal sense of direction and the current direction indicated by newly visible familiar landmarks. This surprising finding may reflect a means of learning about the direction and reliability of landmarks. We show how the mechanism underlying this compromise process might work, and suggest it might also apply to other senses. Contact: Dr Kathryn Jeffery, UCL, [email protected]
A theoretical account of cue averaging in the rodent head direction system URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0283 [OPEN ACCESS] by Page, Hector; Walters, Daniel; Knight, Rebecca; Piette, Caitlin; Jeffery, Kathryn; Stringer, Simon
This paper explores how information from different sources, vision and head rotation, influences the brain’s tracking of head direction, a crucial navigational sub-process. This is an example of sensory integration, which is a fundamental aspect of cognition. We explore this in situations where these signals contradict one another, and suggest that, in order to accurately track head direction, these signals are combined on the basis of how much they differ and their perceived reliability. We use computer simulations based directly on data recorded from the rat brain. This is an interdisciplinary collaboration within Neuroscience, showing the strength of such collaborations. Contact: Mr Hector Page, University of Oxford, [email protected]
Theta phase precession of grid and place cell firing in open environments URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0532 [OPEN ACCESS] by Jeewajee, Ali; Barry, Caswell; Douchamps, Vincent; Manson, Daniel; Lever, Colin; Burgess, Neil
Neurons in the brains of foraging rodents indicates the animal's spatial location by both the rate at which they emit electrical signals ("spikes"), and by the timing of these signals relative to a large oscillation of around 8Hz in the background electrical field (the "theta rhythm"). We characterised how spatial information is signalled by spike timing as rats forage in open arenas, focussing on "place cells" (which fire spikes whenever the rat enters a single place) and "grid cells" (which fire spikes whenever the rat enters any one of several locations arranged in a grid across the environment). Contact: Dr Neil Burgess, UCL, [email protected]
Boundary coding in the rat subiculum URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0514 [OPEN ACCESS] by Stewart, Sarah; Jeewajee, Ali; Wills, Thomas; Burgess, Neil; Lever, Colin
The hippocampus supports spatial mapping derived from two sets of information; one based on the external environment, and one on self motion. We characterise the spatial correlates of subicular ‘boundary vector cells’ (BVCs), which code space relative to boundaries in the external environmental. BVCs typically treat drop-type edges (like cliff edges) similarly to walls, including exhibiting extra fields when additional boundaries are added to the explorable environment. Thus, BVCs treat both kinds of edge as environmental boundaries, despite their dissimilar sensory properties. We also report the existence of ‘boundary off cells’, a new class of boundary-coding cell. Contact: Dr Colin Lever, Durham University, [email protected]
Network mechanisms of grid cells URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0511 [OPEN ACCESS] by Moser, Edvard; Moser, May-Britt; Roudi, Yasser
The discovery of grid cells, and their functional organization, opens the door to some of the first insights into the workings of the association cortices, at a stage of neural processing where firing properties are shaped not primarily by the nature of incoming sensory signals but rather by internal self-organizing principles. The present paper reviews recent advances in our understanding of the mechanisms of grid-cell formation which suggest that the pattern originates by competitive neural- network interactions. Contact: Prof. Edvard Moser, Norwegian University of Science and Technology, [email protected], 73598278
How to build a grid cell URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0520 [OPEN ACCESS] by Schmidt-Hieber, Christoph; Hausser, Michael
Understanding how the brain represents space and enables navigation is one of the most fundamental problems in neuroscience. A population of neurons in the entorhinal cortex fire action potentials at regular spatial intervals, creating a striking grid-like pattern of spike rates which span the whole environment of a navigating animal. This remarkable spatial code may represent a neural map which is crucial for spatial navigation. This review summarizes the latest results from grid cell recordings and discusses the insights they provide for understanding the cellular and network “building blocks” of grid cells in the mammalian brain. Contact: Dr Michael Hausser, University College London, [email protected]
Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0523 by Hasselmo, Michael
Data shows a relationship of cellular resonance and network oscillatory dynamics in the entorhinal cortex to the spatial periodicity of grid cells. This paper presents a model that simulates the resonance and rebound spiking properties of entorhinal neurons to generate spatial periodicity dependent upon phase of input from medial septum. The model shows that a difference in spatial periodicity can result from a difference in neuronal resonance frequency that replicates data from several studies. The model also demonstrates a functional role for the phenomenon of theta cycle skipping in the medial entorhinal cortex. Contact: Prof. Michael Hasselmo, Boston University, [email protected], 617-353-1397
Oscillatory neurocomputing with ring attractors: A network architecture for mapping locations in space onto patterns of neural synchrony URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0526 [OPEN ACCESS] by Blair, Hugh; Wu, Allan; Cong, Jason
Theories of neural coding seek to explain how states of the world are mapped onto states of the brain. Here, we describe a formal theory to hypothesize how information about an animal's location in space is encoded by neural oscillators in the brain. Contact: Prof. Hugh Blair, UCLA, [email protected], (310) 985-3755
Optimal configurations of spatial scale for grid cell firing under noise and uncertainty URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0290 [OPEN ACCESS] by Towse, Benjamin; Barry, Caswell; Bush, Daniel; Burgess, Neil
Grid cells are a type of brain cell whose regular grid-like activation patterns over space encode the animal's current location in the environment. We used a computer simulation to examine how activation patterns of different spatial scale should be organised to best encode location. We found that groups of grids of similar sizes organised in a geometric series (each larger than the last by a fixed ratio) accurately encode location over large ranges, despite noise over time in cell activity. Expanding the grid scales improved accuracy in the face of spatial noise, potentially explaining why grids expand in new environments. Contact: Dr Caswell Barry, UCL, [email protected]
Coordinated learning of grid cell and place cell spatial and temporal properties: multiple scales, attention, and oscillations URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0524 by Grossberg, Stephen; Pilly, Praveen
How do humans and animal learn to navigate in the world? This article describes a neural model which clarifies how this happens as a human or animal navigates along realistic trajectories. The model suggests how space and time may be processed by similar mechanisms ("neural relativity") and how grid cells in the entorhinal cortex and place cells in the hippocampus may both develop using the same laws, despite their different properties. The model proposes how attention may stabilize learned spatial memories, how grid properties may become disorganized without attention, and how oscillatory dynamics may arise from learning and attentional mechanisms. Contact: Prof. Stephen Grossberg, Boston University, [email protected]
How environment geometry affects grid cell symmetry and what we can learn from it URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0188 [OPEN ACCESS] by Krupic, Julija; Bauza, Marius; Burton, Stephen; Lever, Colin; O'Keefe, John
The hippocampal formation provides neuronal representations of environmental location, but the underlying mechanisms are unclear. Grids cells exhibit hexagonal symmetry and form an important subset of this more general class. Occasional changes between hexagonal and non-hexagonal firing patterns imply a common underlying mechanism. Importantly, the symmetrical properties are strongly affected by the geometry of the environment. Here we introduce a field-boundary- interaction model where we demonstrate that the grid cell pattern can be formed from competing place-like and boundary inputs. We show that the modelling results can accurately capture our current experimental observations. Contact: Dr Julija Krupic, UCL, [email protected]
An isomorphic mapping hypothesis of the grid representation URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0521 [OPEN ACCESS] by Brecht, Michael; Ray, Saikat; Burgalossi, Andrea; Tang, Qiusong; Schmidt, Helene; Naumann, Robert
Grid cells, a major building block of the spatial navigation system of the mammalian brain, discharge in a regular grid pattern in space. We propose a model according to which this 'grid attached by neurons to the world' is generated by a neuronal grid in the brain. Contact: Dr Michael Brecht, Humboldt Universitaet zu Berlin, [email protected]
Temporal redistribution of inhibition over neuronal subcellular domains underlies state- dependent rhythmic change of excitability in the hippocampus URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0518 [OPEN ACCESS] by Somogyi, Peter; Katona, Linda; Klausberger, Thomas; Lasztóczi, Balint; Viney, Tim
Explanations of normal and pathological events in the brain require the simultaneous definition of the neuronal organisation in space and time, the chronocircuit. In the last decade, we have focussed on exploring the brain- and network-state dependent activity patterns of identified hippocampal neurons. We discovered a highly specialised spatial and molecular organisation of interneurons, which has also led to the discovery of an unexpected temporal specialisation of GABA release to distinct domains of pyramidal cells. Contact: Prof. Peter Somogyi, MRC Anatomical Neuropharmacology Unit, [email protected]
Theta oscillations decrease spike synchrony in the hippocampus and entorhinal cortex URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0530 by Mizuseki, Kenji; Buzsaki, György
Oscillations and synchrony are often used synonymously. However, oscillatory mechanisms involving both excitation and inhibition can generate non-synchronous yet coordinated firing patterns. Using simultaneous recordings from multiple layers of the entorhinal-hippocampal loop, we found that coactivation of principal cell pairs (synchrony) was lowest during exploration and REM sleep, associated with theta oscillations, and highest in slow wave sleep. Individual principal neurons had a wide range of theta phase preference. Thus, while theta oscillations reduce population synchrony, they nevertheless coordinate the phase (temporal) distribution of neurons. As a result, multiple cell assemblies can nest within the period of the theta cycle. Contact: Prof. György Buzsaki, NYU Neuroscience Institute, [email protected]
Sharp wave/ripple network oscillations and learning-associated hippocampal maps URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0528 by Csicsvari, Jozsef; Dupret, David
Fast oscillatory patterns called Sharp wave/ripple (SWR, 150–250Hz) oscillations usually occur during sleep in hippocampus by measuring local field potentials activty. These SWRs are important for the consolidation of memories. This review discusses how general theories linking SWRs to memory- related function may explain mechanisms related to rodent spatial learning and to the associated stabilisation of new cognitive maps in the hippocampus. Contact: Prof. Jozsef Csicsvari, IST Austria, [email protected]
Selection of preconfigured cell assemblies for representation of novel spatial experiences URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0522 by Dragoi, George; Tonegawa, Susumu
The hippocampus is a brain area necessary for normal internally-generated spatial-temporal representations and its dysfunctions have resulted in anterograde amnesia, impaired imagining of new experiences, and hallucinations. Here we discuss that the place cell sequence of a novel spatial experience is determined, in part, by a selection of a set of cellular firing sequences from a repertoire of existing temporal firing sequences in the hippocampal network. Conceptually, this indicates that novel stimuli from the external world select from their pre-representations rather than construct de novo our internal representations of the world. Contact: Dr George Dragoi, Picower Institute for Learning and Memory at MIT, [email protected]
Hippocampal theta oscillations are slower in humans than in rodents: Implications for models of spatial navigation and memory URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2013.0304 by Jacobs, Joshua
Decades of research in rodents has implicated the 4-8Hz hippocampal theta oscillation as playing a critical role in memory and spatial navigation. However, theta oscillations are rarely observed in humans. I explain this apparent discrepancy by reviewing rare direct brain recordings from neurosurgical patients. This data show that human theta oscillations instead appear at a slower frequency band of 1-4 Hz. This supports theories that theta oscillations are critical for all mammalian memory and navigation, but shows that these signals vary in frequency across species. Contact: Dr Joshua Jacobs, Drexel University, [email protected], 215-895-1860
Neural systems for landmark-based wayfinding in humans URL after publication: http://rstb.royalsocietypublishing.org/lookup/doi/10.1098/rstb.2012.0533 by Epstein, Russell; Vass, Lindsay
Every day we have to find our way from one place to another. How do we do it without getting lost? One strategy is to pay attention to landmarks--things like buildings that don't move and consequently help us figure out where we are in the world and which way we are facing. Recent research reviewed in this paper suggests that landmark-based navigation involves a series of different steps that are supported by neural systems in different parts of the brain. Contact: Prof. Russell Epstein, University of Pennsylvania, [email protected], 215-573-3532