Neural Integrator Models

Integration of information across time is a neural computation of critical importance to a variety of brain functions. Examples include oculomotor neural integrators and head direction cells that integrate velocity signals into positional or directional signals, parametric working memory circuits which convert transient input pulses into self-sustained persistent neural activity patterns, and linear ramping neural activity underlying the accumulation of information during decision making. How is integration over long timescales realized in neural circuits? This article reviews experimental and theoretical work related to this fundamental question, with a focus on the idea that recurrent synaptic or cellular mechanisms can instantiate an integration time much longer than intrinsic biophysical time constants of the system. We first introduce some basic concepts and present two types of codes used by neural integrators – the location code and the rate code. Then we summarize models that implement a variety of candidate mechanisms for neural integration in the brain, and we discuss the problem of fine-tuning of model parameters and possible solutions to this problem. Finally, we outline challenges for future research.

[1]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[2]  H. Sompolinsky,et al.  Temporal integration by calcium dynamics in a model neuron , 2003, Nature Neuroscience.

[3]  A. Fuchs,et al.  Role of cat pontine burst neurons in generation of saccadic eye movements. , 1981, Journal of neurophysiology.

[4]  Xiao-Jing Wang,et al.  Robust Spatial Working Memory through Homeostatic Synaptic Scaling in Heterogeneous Cortical Networks , 2003, Neuron.

[5]  M. Hasselmo,et al.  Graded persistent activity in entorhinal cortex neurons , 2002, Nature.

[6]  H. Sebastian Seung,et al.  Amplification , Attenuation , and Integration 3 4 , 2002 .

[7]  D. Tank,et al.  Persistent neural activity: prevalence and mechanisms , 2004, Current Opinion in Neurobiology.

[8]  M. Hasselmo,et al.  Mechanism of Graded Persistent Cellular Activity of Entorhinal Cortex Layer V Neurons , 2006, Neuron.

[9]  Daniel D. Lee,et al.  Stability of the Memory of Eye Position in a Recurrent Network of Conductance-Based Model Neurons , 2000, Neuron.

[10]  Carlos D. Brody,et al.  Design of Continuous Attractor Networks with Monotonic Tuning Using a Symmetry Principle , 2008, Neural Computation.

[11]  KongFatt Wong-Lin,et al.  Neural Circuit Dynamics Underlying Accumulation of Time-Varying Evidence During Perceptual Decision Making , 2007, Frontiers Comput. Neurosci..

[12]  Stephen C. Cannon,et al.  A proposed neural network for the integrator of the oculomotor system , 1983, Biological Cybernetics.

[13]  Ranulfo Romo,et al.  Basic mechanisms for graded persistent activity: discrete attractors, continuous attractors, and dynamic representations , 2003, Current Opinion in Neurobiology.

[14]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Koulakov,et al.  Model for a robust neural integrator , 2002, Nature Neuroscience.

[16]  Alexandre Pouget,et al.  Digitized neural networks: long-term stability from forgetful neurons , 2002, Nature Neuroscience.

[17]  Xiao-Jing Wang,et al.  Probabilistic Decision Making by Slow Reverberation in Cortical Circuits , 2002, Neuron.

[18]  Ranulfo Romo,et al.  Flexible Control of Mutual Inhibition: A Neural Model of Two-Interval Discrimination , 2005, Science.

[19]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  H. Seung,et al.  Anatomy and discharge properties of pre-motor neurons in the goldfish medulla that have eye-position signals during fixations. , 2000, Journal of neurophysiology.

[21]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[22]  H S Seung,et al.  How the brain keeps the eyes still. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  R. Romo,et al.  A recurrent network model of somatosensory parametric working memory in the prefrontal cortex. , 2003, Cerebral cortex.

[24]  Paul Miller,et al.  Inhibitory control by an integral feedback signal in prefrontal cortex: a model of discrimination between sequential stimuli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Bassett,et al.  Persistent neural activity in head direction cells. , 2003, Cerebral cortex.

[26]  Daniel Durstewitz,et al.  Self-Organizing Neural Integrator Predicts Interval Times through Climbing Activity , 2003, The Journal of Neuroscience.

[27]  Xiao-Jing Wang,et al.  Angular Path Integration by Moving “Hill of Activity”: A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System , 2005, The Journal of Neuroscience.

[28]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[29]  D. Robinson,et al.  Integrating with neurons. , 1989, Annual review of neuroscience.

[30]  Xiao-Jing Wang,et al.  Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks , 2006, Nature Neuroscience.

[31]  H. Seung,et al.  Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron. , 2003, Cerebral cortex.