Spiking and saturating dendrites differentially expand single neuron computation capacity

The integration of excitatory inputs in dendrites is non-linear: multiple excitatory inputs can produce a local depolarization departing from the arithmetic sum of each input's response taken separately. If this depolarization is bigger than the arithmetic sum, the dendrite is spiking; if the depolarization is smaller, the dendrite is saturating. Decomposing a dendritic tree into independent dendritic spiking units greatly extends its computational capacity, as the neuron then maps onto a two layer neural network, enabling it to compute linearly non-separable Boolean functions (lnBFs). How can these lnBFs be implemented by dendritic architectures in practise? And can saturating dendrites equally expand computational capacity? To address these questions we use a binary neuron model and Boolean algebra. First, we confirm that spiking dendrites enable a neuron to compute lnBFs using an architecture based on the disjunctive normal form (DNF). Second, we prove that saturating dendrites as well as spiking dendrites enable a neuron to compute lnBFs using an architecture based on the conjunctive normal form (CNF). Contrary to a DNF-based architecture, in a CNF-based architecture, dendritic unit tunings do not imply the neuron tuning, as has been observed experimentally. Third, we show that one cannot use a DNF-based architecture with saturating dendrites. Consequently, we show that an important family of lnBFs implemented with a CNF-architecture can require an exponential number of saturating dendritic units, whereas the same family implemented with either a DNF-architecture or a CNF-architecture always require a linear number of spiking dendritic units. This minimization could explain why a neuron spends energetic resources to make its dendrites spike.

[1]  J. Magee,et al.  On the Initiation and Propagation of Dendritic Spikes in CA1 Pyramidal Neurons , 2004, The Journal of Neuroscience.

[2]  Bartlett W. Mel,et al.  Pyramidal Neuron as Two-Layer Neural Network , 2003, Neuron.

[3]  Peter L. Hammer,et al.  Boolean Functions - Theory, Algorithms, and Applications , 2011, Encyclopedia of mathematics and its applications.

[4]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.

[5]  R. Silver,et al.  Gap Junctions Compensate for Sublinear Dendritic Integration in an Inhibitory Network , 2012, Science.

[6]  Christof Koch,et al.  Biophysics of Computation: Information Processing in Single Neurons (Computational Neuroscience Series) , 1998 .

[7]  Bartlett W. Mel,et al.  Dendrites: bug or feature? , 2003, Current Opinion in Neurobiology.

[8]  Bartlett W. Mel,et al.  Computational subunits in thin dendrites of pyramidal cells , 2004, Nature Neuroscience.

[9]  Wolfgang Maass,et al.  Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons , 2011, The Journal of Neuroscience.

[10]  Boris S. Gutkin,et al.  Democracy-Independence Trade-Off in Oscillating Dendrites and Its Implications for Grid Cells , 2010, Neuron.

[11]  Dieter van Melkebeek,et al.  Complexity of Boolean Functions, 12.03. - 17.03.2006 , 2006, Complexity of Boolean Functions.

[12]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

[13]  Peter Bro Miltersen,et al.  On converting CNF to DNF , 2005, Theor. Comput. Sci..

[14]  W. Pitts,et al.  A Logical Calculus of the Ideas Immanent in Nervous Activity (1943) , 2021, Ideas That Created the Future.

[15]  Judit K. Makara,et al.  Compartmentalized dendritic plasticity and input feature storage in neurons , 2008, Nature.

[16]  A. Roskies The Binding Problem , 1999, Neuron.

[17]  L. Cathala,et al.  Thin Dendrites of Cerebellar Interneurons Confer Sublinear Synaptic Integration and a Gradient of Short-Term Plasticity , 2012, Neuron.

[18]  Peter L. Hammer,et al.  Boolean Functions , 2013, Discrete Applied Mathematics.

[19]  Hongbo Jia,et al.  Dendritic organization of sensory input to cortical neurons in vivo , 2010, Nature.