Storage of Correlated Patterns in Standard and Bistable Purkinje Cell Models

The cerebellum has long been considered to undergo supervised learning, with climbing fibers acting as a ‘teaching’ or ‘error’ signal. Purkinje cells (PCs), the sole output of the cerebellar cortex, have been considered as analogs of perceptrons storing input/output associations. In support of this hypothesis, a recent study found that the distribution of synaptic weights of a perceptron at maximal capacity is in striking agreement with experimental data in adult rats. However, the calculation was performed using random uncorrelated inputs and outputs. This is a clearly unrealistic assumption since sensory inputs and motor outputs carry a substantial degree of temporal correlations. In this paper, we consider a binary output neuron with a large number of inputs, which is required to store associations between temporally correlated sequences of binary inputs and outputs, modelled as Markov chains. Storage capacity is found to increase with both input and output correlations, and diverges in the limit where both go to unity. We also investigate the capacity of a bistable output unit, since PCs have been shown to be bistable in some experimental conditions. Bistability is shown to enhance storage capacity whenever the output correlation is stronger than the input correlation. Distribution of synaptic weights at maximal capacity is shown to be independent on correlations, and is also unaffected by the presence of bistability.

[1]  James V. Stone,et al.  Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  Y. Prigent [Long term depression]. , 1989, Annales medico-psychologiques.

[3]  Michael Häusser,et al.  Membrane potential bistability is controlled by the hyperpolarization‐activated current IH in rat cerebellar Purkinje neurons in vitro , 2002, The Journal of physiology.

[4]  D. Amit,et al.  Perceptron learning with sign-constrained weights , 1989 .

[5]  Yoshiko Kojima,et al.  Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning? , 2008, Journal of neurophysiology.

[6]  E. Gardner The space of interactions in neural network models , 1988 .

[7]  Alain Marty,et al.  Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states , 2010, Proceedings of the National Academy of Sciences.

[8]  J. Nadal,et al.  What can we learn from synaptic weight distributions? , 2007, Trends in Neurosciences.

[9]  J. Nadal,et al.  Optimal Information Storage and the Distribution of Synaptic Weights Perceptron versus Purkinje Cell , 2004, Neuron.

[10]  H. Sompolinsky,et al.  Bistability of cerebellar Purkinje cells modulated by sensory stimulation , 2005, Nature Neuroscience.

[11]  Thomas M. Cover,et al.  Geometrical and Statistical Properties of Systems of Linear Inequalities with Applications in Pattern Recognition , 1965, IEEE Trans. Electron. Comput..

[12]  H. Gutfreund,et al.  Capacity of neural networks with discrete synaptic couplings , 1990 .

[13]  Ray W Turner,et al.  Firing dynamics of cerebellar purkinje cells. , 2007, Journal of neurophysiology.

[14]  Jean-Pierre Nadal On the storage capacity with sign-constrained synaptic couplings , 1990 .

[15]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[16]  Ido Kanter,et al.  On the capacity per synapse , 1990 .

[17]  Marvin Minsky,et al.  Perceptrons: An Introduction to Computational Geometry , 1969 .

[18]  J. Albus A Theory of Cerebellar Function , 1971 .

[19]  John Porrill,et al.  Cerebellar Motor Learning: When Is Cortical Plasticity Not Enough? , 2007, PLoS Comput. Biol..

[20]  A. A. Mullin,et al.  Principles of neurodynamics , 1962 .

[21]  R. Palmer,et al.  Introduction to the theory of neural computation , 1994, The advanced book program.

[22]  Henrik Jörntell,et al.  Synaptic Memories Upside Down: Bidirectional Plasticity at Cerebellar Parallel Fiber-Purkinje Cell Synapses , 2006, Neuron.

[23]  D. Widmaier,et al.  Sign-constrained linear learning and diluting in neural networks , 1991 .

[24]  John Porrill,et al.  Sensory Prediction or Motor Control? Application of Marr–Albus Type Models of Cerebellar Function to Classical Conditioning , 2010, Front. Comput. Neurosci..

[25]  M. Yartsev,et al.  Pausing Purkinje Cells in the Cerebellum of the Awake Cat , 2008, Front. Syst. Neurosci..

[26]  Bruno Delord,et al.  A biophysical model of nonlinear dynamics underlying plateau potentials and calcium spikes in purkinje cell dendrites. , 2002, Journal of neurophysiology.

[27]  M. Häusser,et al.  Integration of quanta in cerebellar granule cells during sensory processing , 2004, Nature.

[28]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[29]  B. Barbour,et al.  Properties of Unitary Granule Cell→Purkinje Cell Synapses in Adult Rat Cerebellar Slices , 2002, The Journal of Neuroscience.

[30]  E. D’Angelo,et al.  Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum , 2001, Nature Neuroscience.

[31]  H. Sompolinsky,et al.  Purkinje cells in awake behaving animals operate at the upstate membrane potential , 2006, Nature Neuroscience.