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      The Development of the Head Direction System before Eye Opening in the Rat

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          Summary

          Head direction (HD) cells are neurons found in the hippocampal formation and connected areas that fire as a function of an animal’s directional orientation relative to its environment [ 1, 2]. They integrate self-motion and environmental sensory information to update directional heading [ 3]. Visual landmarks, in particular, exert strong control over the preferred direction of HD cell firing [ 4]. The HD signal has previously been shown to appear adult-like as early as postnatal day 16 (P16) in the rat pup, just after eye opening and coinciding with the first spontaneous exploration of its environment [ 5, 6]. In order to determine whether the HD circuit can begin its organization prior to the onset of patterned vision, we recorded from the anterodorsal thalamic nucleus (ADN) and its postsynaptic target in the hippocampal formation, the dorsal pre-subiculum (PrSd), before and after eye opening in pre-weanling rats. We find that HD cells can be recorded at the earliest age sampled (P12), several days before eye opening. However, this early HD signal displays low directional information content and lacks stability both within and across trials. Following eye opening, the HD system matures rapidly, as more cells exhibit directional firing, and the quality and reliability of the directional signal improves dramatically. Cue-rotation experiments show that a prominent visual landmark is able to control HD responses within 24 hr of eye opening. Together, the results suggest that the directional network can be organized independently of visual spatial information while demonstrating the importance of patterned vision for accurate and reliable orientation in space.

          Highlights

          • Head direction (HD) cells exist at least 3 days before eye opening in rats
          • HD signals improve sharply at eye opening and mature rapidly thereafter
          • Visual inputs can exert control over the HD system soon after eye opening

          Abstract

          Tan et al. reveal the existence of head direction (HD) cells several days before eye opening in the rat pup, suggesting that the HD cell network can be organized independently of patterned vision. The stability and directional tuning of HD cells improve sharply at eye opening, demonstrating the importance of vision for accurate navigation.

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          Most cited references 31

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          Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis.

          This paper is a study of the behavioral and spatial firing correlates of neurons in the rat postsubiculum. Recordings were made from postsubicular neurons as rats moved freely throughout a cylindrical chamber, where the major cue for orientation was a white card taped to the inside wall. An automatic video/computer system monitored cell discharge while simultaneously tracking the position of 2 colored light emitting diodes (LEDs) secured to the animal's head. The animal's location was calculated from the position of one of the LEDs and head direction in the horizontal plane calculated from the relative positions of the 2 LEDs. Approximately 26% of the cells were classified as head-direction cells because they discharged as a function of the animal's head direction in the horizontal plane, independent of the animal's behavior, location, or trunk position. For each head-direction cell, vectors drawn in the direction of maximal firing were parallel throughout the recording chamber and did not converge toward a single point. Plots of firing rate versus head direction showed that each firing-rate/head-direction function was adequately described by a triangular function. Each cell's maximum firing rate occurred at only one (the preferred) head direction; firing rates at head directions on either side of the preferred direction decreased linearly with angular deviation from the preferred direction. Results from 24 head-direction cells in 7 animals showed an equal distribution of preferred firing directions over a 360 degrees angle. The peak firing rate of head-direction cells varied from 5 to 115 spikes/sec (mean: 35). The range of head-direction angles over which discharge was elevated (directional firing range) was usually about 90 degrees, with little, if any, discharge at head directions outside this range. Quantitative analysis showed the location of the animal within the cylinder had minimal effect on directional cell firing. For each head-direction cell, the preferred direction, peak firing rate, and directional firing range remained stable for days. These results identify a new cell type that signals the animal's head direction in its environment.
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            Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements.

            Simultaneous recording from large numbers of neurons is a prerequisite for understanding their cooperative behavior. Various recording techniques and spike separation methods are being used toward this goal. However, the error rates involved in spike separation have not yet been quantified. We studied the separation reliability of "tetrode" (4-wire electrode)-recorded spikes by monitoring simultaneously from the same cell intracellularly with a glass pipette and extracellularly with a tetrode. With manual spike sorting, we found a trade-off between Type I and Type II errors, with errors typically ranging from 0 to 30% depending on the amplitude and firing pattern of the cell, the similarity of the waveshapes of neighboring neurons, and the experience of the operator. Performance using only a single wire was markedly lower, indicating the advantages of multiple-site monitoring techniques over single-wire recordings. For tetrode recordings, error rates were increased by burst activity and during periods of cellular synchrony. The lowest possible separation error rates were estimated by a search for the best ellipsoidal cluster shape. Human operator performance was significantly below the estimated optimum. Investigation of error distributions indicated that suboptimal performance was caused by inability of the operators to mark cluster boundaries accurately in a high-dimensional feature space. We therefore hypothesized that automatic spike-sorting algorithms have the potential to significantly lower error rates. Implementation of a semi-automatic classification system confirms this suggestion, reducing errors close to the estimated optimum, in the range 0-8%.
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              The head direction signal: origins and sensory-motor integration.

              Navigation first requires accurate perception of one's spatial orientation within the environment, which consists of knowledge about location and directional heading. Cells within several limbic system areas of the mammalian brain discharge allocentrically as a function of the animal's directional heading, independent of the animal's location and ongoing behavior. These cells are referred to as head direction (HD) cells and are believed to encode the animal's perceived directional heading with respect to its environment. Although HD cells are found in several areas, the principal circuit for generating this signal originates in the dorsal tegmental nucleus and projects serially, with some reciprocal connections, to the lateral mammillary nucleus --> anterodorsal thalamus --> PoS, and terminates in the entorhinal cortex. HD cells receive multimodal information about landmarks and self-generated movements. Vestibular information appears critical for generating the directional signal, but motor/proprioceptive and landmark information are important for updating it.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                16 February 2015
                16 February 2015
                : 25
                : 4
                : 479-483
                Affiliations
                [1 ]Cell and Developmental Biology, University College London, London WC1E 6BT, UK
                [2 ]Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, UK
                [3 ]Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London, London WC1E 6BT, UK
                Author notes
                []Corresponding author f.cacucci@ 123456ucl.ac.uk
                [∗∗ ]Corresponding author t.wills@ 123456ucl.ac.uk
                [4]

                Co-first author

                [5]

                Co-senior author

                Article
                S0960-9822(14)01633-9
                10.1016/j.cub.2014.12.030
                4331281
                25660541
                © 2015 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

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                Life sciences

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