Rats Generate Vibrissal Sensory Evidence until Boundary Crossing Triggers a Decision

Behaviors in which primates collect externally generated streams of sensory evidence, such as judgment of random dot motion direction, are explained by a bounded integration decision model. Does this model extend to rodents, and does it account for behavior in which the motor system generates evidence through interactions with the environment? In this study, rats palpated surfaces to identify the texture before them, showing marked trial-to-trial variability in the number of touches prior to expressing their choice. By high-speed video, we tracked whisker kinematic features and characterized how they encoded the contacted texture. Next, we quantified the evidence for each candidate texture transmitted on each touch by the specified whisker kinematic features. The instant of choice was well fit by modeling the brain as an integrator that gives the greatest weight to vibrissal evidence on first touch and exponentially less weight to evidence on successive touches; according to this model, the rat makes a decision when the accumulated quantity of evidence for one texture reaches a boundary. In summary, evidence appears to be accumulated within the brain until sufficient to support a well-grounded choice. These findings extend the framework of bounded sensory integration from primates to rodents and from passively received evidence to evidence that is actively generated by the sensorimotor system.

[1]  Dori Derdikman,et al.  Pre-neuronal morphological processing of object location by individual whiskers , 2013, Nature Neuroscience.

[2]  Andrej Kosir,et al.  Unsupervised quantification of whisking and head movement in freely moving rodents. , 2011, Journal of neurophysiology.

[3]  G. Brier VERIFICATION OF FORECASTS EXPRESSED IN TERMS OF PROBABILITY , 1950 .

[4]  M. Diamond,et al.  Neuronal Encoding of Texture in the Whisker Sensory Pathway , 2005, PLoS biology.

[5]  Alexei A. Koulakov,et al.  A primacy code for odor identity , 2017, Nature Communications.

[6]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. Fisher THE USE OF MULTIPLE MEASUREMENTS IN TAXONOMIC PROBLEMS , 1936 .

[8]  Maurice Merleau-Ponty Phenomenology of Perception , 1964 .

[9]  E. Arabzadeh,et al.  A comparison of neuronal and behavioral detection and discrimination performances in rat whisker system. , 2011, Journal of neurophysiology.

[10]  Roozbeh Kiani,et al.  Neural Mechanisms of Post-error Adjustments of Decision Policy in Parietal Cortex , 2016, Neuron.

[11]  Milo E. Richmond,et al.  Influence of Soil Texture, Moisture and Temperature on Nest-site Selection and Burrowing by the Pine Vole, Microtus pinetorum , 1985 .

[12]  Mathew H. Evans,et al.  What the Whiskers Tell the Brain , 2018, Neuroscience.

[13]  Philippe Lefèvre,et al.  Surface strain measurements of fingertip skin under shearing , 2016, Journal of The Royal Society Interface.

[14]  E. Ahissar,et al.  Perception as a closed-loop convergence process , 2016, eLife.

[15]  Vinzenz H. Schönfelder,et al.  Transformation of Perception from Sensory to Motor Cortex , 2017, Current Biology.

[16]  David J. Hand,et al.  A Simple Generalisation of the Area Under the ROC Curve for Multiple Class Classification Problems , 2001, Machine Learning.

[17]  M. Diamond,et al.  Sensory Prioritization in Rats: Behavioral Performance and Neuronal Correlates , 2016, The Journal of Neuroscience.

[18]  Masakazu Konishi,et al.  The Role of Auditory Feedback in Birdsong , 2004, Annals of the New York Academy of Sciences.

[19]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[20]  R. Rajan,et al.  Laminar‐specific encoding of texture elements in rat barrel cortex , 2017, The Journal of physiology.

[21]  Hannes P. Saal,et al.  Spatial and temporal codes mediate the tactile perception of natural textures , 2014, 2014 IEEE Haptics Symposium (HAPTICS).

[22]  R. Azouz,et al.  Mechanisms of Tactile Information Transmission through Whisker Vibrations , 2009, The Journal of Neuroscience.

[23]  Daniel N. Hill,et al.  Texture Coding in the Rat Whisker System: Slip-Stick Versus Differential Resonance , 2008, PLoS biology.

[24]  Mathew E. Diamond,et al.  Texture Identification by Bounded Integration of Sensory Cortical Signals , 2019, Current Biology.

[25]  Mathew E Diamond,et al.  Whisking and whisker kinematics during a texture classification task , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  Wieland Brendel,et al.  Biomechanical Texture Coding in Rat Whiskers , 2018, Scientific Reports.

[27]  C. R. Rao,et al.  The Utilization of Multiple Measurements in Problems of Biological Classification , 1948 .

[28]  Timothy D. Hanks,et al.  Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment , 2008, The Journal of Neuroscience.

[29]  O. Johansson,et al.  Immunohistochemical evidence for the presence of somatostatin-containing sensory nerve fibres in the human skin , 1987, Neuroscience Letters.

[30]  Rune W. Berg,et al.  Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. , 2003, Journal of neurophysiology.

[31]  Cornelius Schwarz,et al.  Responses of rat trigeminal ganglion neurons to longitudinal whisker stimulation. , 2008, Journal of neurophysiology.

[32]  M. Diamond,et al.  Complementary Contributions of Spike Timing and Spike Rate to Perceptual Decisions in Rat S1 and S2 Cortex , 2015, Current Biology.

[33]  Jason Wolfe,et al.  Sparse temporal coding of elementary tactile features during active whisker sensation , 2009, Nature Neuroscience.

[34]  Shantanu P. Jadhav,et al.  Psychometric Curve and Behavioral Strategies for Whisker-Based Texture Discrimination in Rats , 2011, PloS one.

[35]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.