Abstract
The human channel capacity for identifying sensory stimuli is compared with channel capacities based on neurophysiological findings. Studies have shown that cells in the postsubiculum (PoS) and the anterior dorsal thalamus (ADN) of the rat discharge as a function of the animal’s head direction in the horizontal plane. We compute the statistical properties of the firing rates of head direction (HD) cells and the potential amount of information transmitted by these cells according to two theoretical models. Thecell response model for single cells indicates that information transmitted is much less than 0.5 bits. Thepopulation response model developed for cell ensembles generates values in the range of 1–3.2 bits, suggesting that a cell population can distinguish between two and nine head directions, depending on the value used for the standard deviation of directions over which a cell fires. These values are similar to those found in human psychophysical studies of the channel capacity for unidimensional sensory attributes.
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Arbib, M. A., Érdi, P., &Szentágothai, J. (1998).Neural organization: Structure, function, and dynamics. Cambridge, MA: MIT press.
Attneave, F. (1959).Applications of information theory to psychology. New York: Holt, Rinehart & Winston.
Baird, J. C. (1984). Information theory and information processing.Information Processing & Management,20, 373–381.
Baird, J. C. (1997).Sensation and judgment: Complementarity theory of psychophysics. Mahwah, NJ: Erlbaum.
Baird, J. C., &Noma, E. (1978).Fundamentals of scaling and psychophysics. New York: Wiley.
Barlow, H. (1995). The neuron doctrine in perception. In M. S. Gazzaniga (Ed.),The cognitive neurosciences (pp. 415–435). Cambridge, MA: MIT Press, Bradford Books.
Blair, H. T., &Sharp, P. E. (1995). Anticipatory head direction signals in anterior thalamus: Evidence for a thalamocortical circuit that integrates angular head motion to compute head direction.Journal of Neuroscience,15, 6260–6270.
Chen, L. L., Lin, L. H., Green, E. J., Barnes, C.A., &McNaughton, B. L. (1994). Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation.Experimental Brain Research,101, 8–23.
Cover, T. M., &Thomas, J. A. (1991).Elements of information theory. New York: Wiley.
Dudchenko, P. A., &Taube, J. S. (1997). Correlation between head direction cell activity and spatial behavior on a radial arm maze.Behavioral Neuroscience,111, 3–19.
Eriksen, C. W., &Hake, H. W. (1955). Multidimensional stimulus differences and accuracy of discrimination.Journal of Experimental Psychology,50, 153–160.
Fisher, N. I. (1993).Statistical analysis of circular data. Cambridge: Cambridge University Press.
Garner, W. R. (1962).Uncertainty and structure as psychological concepts. New York: Wiley.
Georgopoulos, A. P. (1995). Motor cortex and cognitive processing. In M. S. Gazzaniga (Ed.),The cognitive neurosciences (pp. 507–517). Cambridge, MA: MIT Press, Bradford Books.
Georgopoulos, A. P., Caminiti, R., Kalaska, J. F., &Massey, J. T. (1983). Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations.Experimental Brain Research,7, 327–336.
Georgopoulos, A. P., &Massey, J. T. (1988). Cognitive spatial motor processes: 2. Information transmitted by the direction of twodimensional arm movements and by neuronal populations in primate motor cortex and area 5.Experimental Brain Research,69, 315–326.
Gershon, E. D., Wiener, M. C., Latham, P. E., &Richmond, B. J. (1998). Coding strategies in monkey V1 and inferior temporal cortices.Journal of Neurophysiology,79, 1135–1144.
Gothard, K. M., Skaggs, W. E., Moore, K. M., &McNaughton, B. L. (1996). Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task.Journal of Neuroscience,16, 823–835.
Jung, M. W., &McNaughton, B. L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer.Hippocampus,3, 165–182.
Jung, M. W., Wiener, S. I., &McNaughton, B. L. (1994). Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat.Journal of Neuroscience,14, 7347–7356.
Katz, B. (1966).Nerve, muscle, and synapse. New York: McGraw-Hill.
MacKay, D. M., &McCulloch, W. S. (1952). The limiting information capacity of a neuronal link.Bulletin of Mathematical Biophysics,14, 127–135.
Markus, E. J., Barnes, C. A., McNaughton, B. L., Gladden, V. L., &Skaggs, W. E. (1994). Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input.Hippocampus,4, 410–421.
Miller, G. A. (1956). The magical number seven, plus or minus two: Some limits on capacity for processing information.Psychological Review,63, 81–97.
Miller, J. P., Jacobs, G. A., &Theunissen, F. E. (1991). Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons.Journal of Neurophysiology,66, 1680–1689.
Mizumori, S. J. Y., &Williams, J. D. (1993). Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats.Journal of Neuroscience,13, 4015–4028.
Muller, R. U. (1996). A quarter of a century of place cells.Neuron,17, 813–822.
Norwich, K. H. (1993).Information, sensation, and perception. New York: Academic Press.
O’Keefe, J., &Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat.Brain Research,34, 171–175.
O’Keefe, J., &Nadel, L. (1978).The hippocampus as a cognitive map. Oxford: Oxford University Press, Clarendon Press.
Olton, D. S., Collison, C., &Werz, M. A. (1977). Spatial memory and radial arm maze performance of rats.Learning & Motivation,8, 289–314.
O’Mara, S. M. (1995). Spatially selective firing properties of hippocampal formation neurons in rodents and primates.Progress in Neurobiology,45, 253–274.
Optican, L. M., &Richmond, B. J. (1987). Temporal encoding of twodimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis.Journal of Neurophysiology,57, 162–178.
Poucet, B., Thinus-Blanc, C., &Muller, R. U. (1994). Place cells in the ventral hippocampus of rats.Neuroreport,5, 2045–2048.
Richmond, B. J., &Optican, L. M. (1990). Temporal encoding of twodimensional patterns by single units in primate visual cortex: II. Information transmission.Journal of Neurophysiology,64, 370–380.
Rieke, F., Warland, D., de Ruyter van Stevenink, R., &Bialek,W. (1997).Spikes: Exploring the neural code. Cambridge, MA: MIT Press.
Shannon, C. E., Weaver, W. (1963).The mathematical theory of communication. Urbana: University of Illinois Press.
Skaggs, W. E., McNaughton, B. L., Gothard, K. M., &Markus, E. J. (1993). An information-theoretic approach to deciphering the hippocampal code.Advances in Neural Information Processing Systems,5, 1030–1037.
Stackman, R. W., &Taube, J. S. (1997). Firing properties of head direction cells in rat anterior thalamic neurons: Dependence upon vestibular input.Journal of Neuroscience,17, 4349–4358.
Stackman, R. W., &Taube, J. S. (1998). Firing properties of cells recorded in the lateral mammillary nuclei of rats: Head direction, angular velocity, and pitch cells.Journal of Neuroscience,18, 9020–9037.
Taube, J. S. (1995a). Head direction cells recorded in the anterior thalamic nuclei of freely moving rats.Journal of Neuroscience,15, 70–86.
Taube, J. S. (1995b). Place cells recorded in the parasubiculum of freely-moving rats.Hippocampus,5, 569–583.
Taube, J. S. (1998). Head direction cells and the neurophysiological basis for a sense of direction.Progress in Neurobiology,55, 225–256.
Taube, J. S., &Burton, H. L. (1995). Head direction cell activity monitored in a novel environment and during a cue conflict situation.Journal of Neurophysiology,74, 1953–1971.
Taube, J. S., &Muller, R. U. (1998). Comparison of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats.Hippocampus,8, 87–108.
Taube, J. S., Muller, R. U., &Ranck, J. B., Jr. (1990a). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis.Journal of Neuroscience,10, 420–435.
Taube, J. S., Muller, R. U., &Ranck, J. B., Jr. (1990b). Head-direction cells recorded from the postsubiculum in freely moving rats: II. Effects of environmental manipulations.Journal of Neuroscience,10, 436–447.
Taube, J. S., Stackman, R. W., &Dudchenko, P. A. (1996). Headdirection cell activity monitored following passive transport into a novel environment.Society for Neuroscience Abstracts,22, 1873.
Theunissen, F. E., &Miller, J. P. (1991). Representation of sensory information in the cricket cercal sensory system: II. Information theoretic calculation of system accuracy and optimal tuning-curve widths of four primary interneurons.Journal of Neurophysiology,66, 1690–1703.
Tolman, E. C., Ritchie, B. G., &Kalish, D. (1946). Studies in spatial learning: I. Orientation and the short-cut.Journal of Experimental Psychology,36, 13–24.
Tovée, M. J., Rolls, E. T., Treves, A., &Bellis, R. P. (1993). Information encoding and the responses of single neurons in the primate temporal visual cortex.Journal of Neurophysiology,70, 640–654.
Wiener, S. I. (1993). Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task.Journal of Neuroscience,13, 3802–3817.
Wilson, M. A., &McNaughton, B. L. (1993). Dynamics of the hippocampal ensemble code for space.Science,261, 1055–1058.
Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: A theory.Journal of Neuroscience,16, 2112–2126.
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This work was supported by NIMH Grants MH48924 and MH01286 to J.S.T.
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Baird, J.C., Taube, J.S. & Peterson, D.V. Statistical and information properties of head direction cells. Perception & Psychophysics 63, 1026–1037 (2001). https://doi.org/10.3758/BF03194521
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DOI: https://doi.org/10.3758/BF03194521