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      A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations


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          Learning the spatial organization of the environment is essential for most animals’ survival. This requires the animal to derive allocentric spatial information from egocentric sensory and motor experience. The neural mechanisms underlying this transformation are mostly unknown. We addressed this problem in electric fish, which can precisely navigate in complete darkness and whose brain circuitry is relatively simple. We conducted the first neural recordings in the preglomerular complex, the thalamic region exclusively connecting the optic tectum with the spatial learning circuits in the dorsolateral pallium. While tectal topographic information was mostly eliminated in preglomerular neurons, the time-intervals between object encounters were precisely encoded. We show that this reliable temporal information, combined with a speed signal, can permit accurate estimation of the distance between encounters, a necessary component of path-integration that enables computing allocentric spatial relations. Our results suggest that similar mechanisms are involved in sequential spatial learning in all vertebrates.

          eLife digest

          Finding their way around is an essential part of survival for many animals and helps them to locate food, mates and shelter. Animals have evolved the ability to form a 'map' or representation of their surroundings. For example, the electric fish Apteronotus leptorhynchus, is able to precisely learn the location of food and navigate there. It can do this in complete darkness by generating a weak electric field. As it swims, every object it encounters generates an ‘electric image’ that is detected on the skin and processed in the brain.

          However, all the cues the fish comes across are from its own point of view – the information about its environment is processed with respect to its location. And yet, the map that it generates needs to be independent of the fish’s position – it has to work regardless of where the animal is. The way animals translate ‘self-centered’ experiences to form a general representation of their surroundings is not yet fully understood.

          Now, Wallach et al. studied how internal brain maps are generated in A. leptorhynchus. Information about the fish's environment passes through a structure in the brain called the preglomerular complex. Measuring the activity of this region revealed that the preglomerular complex does not process much self-centered information. Instead, whenever the fish passed any object – regardless of where it was in relation to the fish – the event triggered a brief burst of preglomerular activity. The intensity of the activity depended on how recently the fish had encountered another object. This information, combined with the dynamics of the fish's movement, could be what allows the fish to convert a sequence of encounters into a general spatial map.

          These findings could help to inform research on learning and navigation. Further research could also reveal whether other species, including humans, generate their mental maps in a similar way. This may be relevant for people suffering from diseases such as Alzheimer’s, in which a sense of orientation has become impaired.

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          Most cited references51

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          Memory, navigation and theta rhythm in the hippocampal-entorhinal system.

          Theories on the functions of the hippocampal system are based largely on two fundamental discoveries: the amnestic consequences of removing the hippocampus and associated structures in the famous patient H.M. and the observation that spiking activity of hippocampal neurons is associated with the spatial position of the rat. In the footsteps of these discoveries, many attempts were made to reconcile these seemingly disparate functions. Here we propose that mechanisms of memory and planning have evolved from mechanisms of navigation in the physical world and hypothesize that the neuronal algorithms underlying navigation in real and mental space are fundamentally the same. We review experimental data in support of this hypothesis and discuss how specific firing patterns and oscillatory dynamics in the entorhinal cortex and hippocampus can support both navigation and memory.
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            Neural dynamics for landmark orientation and angular path integration

            Summary Many animals navigate using a combination of visual landmarks and path integration. In mammalian brains, head direction cells integrate these two streams of information by representing an animal's heading relative to landmarks, yet maintaining their directional tuning in darkness based on self-motion cues. Here we use two-photon calcium imaging in head-fixed flies walking on a ball in a virtual reality arena to demonstrate that landmark-based orientation and angular path integration are combined in the population responses of neurons whose dendrites tile the ellipsoid body — a toroidal structure in the center of the fly brain. The population encodes the fly's azimuth relative to its environment, tracking visual landmarks when available and relying on self-motion cues in darkness. When both visual and self-motion cues are absent, a representation of the animal's orientation is maintained in this network through persistent activity — a potential substrate for short-term memory. Several features of the population dynamics of these neurons and their circular anatomical arrangement are suggestive of ring attractors — network structures proposed to support the function of navigational brain circuits.
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              The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability.

              Although signaling between neurons is central to the functioning of the brain, we still do not understand how the code used in signaling depends on the properties of synaptic transmission. Theoretical analysis combined with patch clamp recordings from pairs of neocortical pyramidal neurons revealed that the rate of synaptic depression, which depends on the probability of neurotransmitter release, dictates the extent to which firing rate and temporal coherence of action potentials within a presynaptic population are signaled to the postsynaptic neuron. The postsynaptic response primarily reflects rates of firing when depression is slow and temporal coherence when depression is fast. A wide range of rates of synaptic depression between different pairs of pyramidal neurons was found, suggesting that the relative contribution of rate and temporal signals varies along a continuum. We conclude that by setting the rate of synaptic depression, release probability is an important factor in determining the neural code.

                Author and article information

                Role: Reviewing Editor
                Role: Senior Editor
                eLife Sciences Publications, Ltd
                22 November 2018
                : 7
                [1 ]deptDepartment of Physics University of Ottawa OttawaCanada
                [2 ]deptDepartment of Cellular and Molecular Medicine University of Ottawa OttawaCanada
                [3 ]deptCenter for Neural Dynamics, Mind and Brain Research Institute University of Ottawa OttawaCanada
                University of Maryland United States
                Brandeis University United States
                University of Maryland United States
                Author notes

                The Zuckerman Institute, Columbia University, New York, United States.


                Center for Computational Mathematics, Flatiron Institute, New York, United States.

                © 2018, Wallach et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                : 18 March 2018
                : 12 November 2018
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: 121891-2009
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000024, Canadian Institutes of Health Research;
                Award ID: 49510
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: 147489-2017
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Research Article
                Custom metadata
                A novel neural mechanism for precise, unbiased estimation of time intervals in the thalamus of electric fish is likely used for computing distance between object encounters.

                Life sciences
                thalamus,path integration,electrosensation,time-coding,spike frequency adaptation,renewal process,other


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