Neural Variability in Premotor Cortex Is Modulated by Trial History and Predicts Behavioral Performance

In the study of decision making, emphasis is placed on different forms of perceptual integration, while the influence of other factors, such as memory, is ignored. In addition, it is believed that the information underlying decision making is carried in the rate of the neuronal response, while its variability is considered unspecific. Here we studied the influence of recent experience on motor decision making by analyzing the activity of neurons in the dorsal premotor area of two monkeys performing a countermanding arm task. We observe that the across-trial variability of the neural response strongly correlates with trial history-dependent changes in reaction time. Using a theoretical model of decision making, we show that a trial history-monitoring signal can explain the observed behavioral and neural modulation. Our study reveals that, in the neural processes that culminate in motor plan maturation, the evidence provided by perception and memory is reflected in mean rate and variance respectively.

[1]  S. Ferraina,et al.  Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys. , 2011, Journal of neurophysiology.

[2]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[3]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[4]  Gustavo Deco,et al.  Neural Network Mechanisms Underlying Stimulus Driven Variability Reduction , 2012, PLoS Comput. Biol..

[5]  P. D. Giudice,et al.  Modelling the formation of working memory with networks of integrate-and-fire neurons connected by plastic synapses , 2003, Journal of Physiology-Paris.

[6]  Leanne Boucher,et al.  Influence of history on saccade countermanding performance in humans and macaque monkeys , 2007, Vision Research.

[7]  V. Stuphorn,et al.  Medial Frontal Cortex Motivates But Does Not Control Movement Initiation in the Countermanding Task , 2010, The Journal of Neuroscience.

[8]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[9]  Leanne Boucher,et al.  Nonindependent and nonstationary response times in stopping and stepping saccade tasks , 2010, Attention, perception & psychophysics.

[10]  Leanne Boucher,et al.  Neural Basis of Adaptive Response Time Adjustment during Saccade Countermanding , 2011, The Journal of Neuroscience.

[11]  Anders Ledberg,et al.  Neurobiological Models of Two-Choice Decision Making Can Be Reduced to a One-Dimensional Nonlinear Diffusion Equation , 2008, PLoS Comput. Biol..

[12]  Pierpaolo Pani,et al.  Inhibitory control of reaching movements in humans , 2009, Experimental Brain Research.

[13]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[14]  G. McCarthy,et al.  Decisions under Uncertainty: Probabilistic Context Influences Activation of Prefrontal and Parietal Cortices , 2005, The Journal of Neuroscience.

[15]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[16]  M. Shadlen,et al.  Decision-making with multiple alternatives , 2008, Nature Neuroscience.

[17]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[18]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[19]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[20]  Martina Rieger,et al.  Inhibitory after‐effects in the stop signal paradigm , 1999 .

[21]  Stefan Rotter,et al.  Measurement of variability dynamics in cortical spike trains , 2008, Journal of Neuroscience Methods.

[22]  Philip L. Smith,et al.  Psychology and neurobiology of simple decisions , 2004, Trends in Neurosciences.

[23]  S. Ishii,et al.  Resolution of Uncertainty in Prefrontal Cortex , 2006, Neuron.

[24]  M. Vink,et al.  On the Role of the Striatum in Response Inhibition , 2010, PloS one.

[25]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[26]  D. G. Albrecht,et al.  Bayesian analysis of identification performance in monkey visual cortex: Nonlinear mechanisms and stimulus certainty , 1995, Vision Research.

[27]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[28]  S Ferraina,et al.  Cortical Networks for Visual Reaching: Intrinsic Frontal Lobe Connectivity , 1996, The European journal of neuroscience.

[29]  G. Logan,et al.  Response inhibition in the stop-signal paradigm , 2008, Trends in Cognitive Sciences.

[30]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[31]  Paul F. M. J. Verschure,et al.  Environmentally mediated synergy between perception and behaviour in mobile robots , 2003, Nature.

[32]  G. Logan.  On the ability to inhibit thought and action , 1984 .

[33]  Gustavo Deco,et al.  The encoding of alternatives in multiple-choice decision making , 2009, Proceedings of the National Academy of Sciences.

[34]  G. Luppino,et al.  ß Federation of European Neuroscience Societies Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey , 2022 .

[35]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

[36]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[37]  F. AbbottPhysics.  Realistic Synaptic Inputs for Model Neural Networks , 1991 .

[38]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[39]  D. P. Hanes,et al.  Controlled Movement Processing: Superior Colliculus Activity Associated with Countermanded Saccades , 2003, The Journal of Neuroscience.

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

[41]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .

[42]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[43]  J. Dreher,et al.  Decision Threshold Modulation in the Human Brain , 2010, The Journal of Neuroscience.