Object-finding skill created by repeated reward experience

For most animals, survival depends on rapid detection of rewarding objects, but search for an object surrounded by many others is known to be difficult and time consuming. However, there is neuronal evidence for robust and rapid differentiation of objects based on their reward history in primates (Hikosaka, Kim, Yasuda, & Yamamoto, 2014). We hypothesized that such robust coding should support efficient search for high-value objects, similar to a pop-out mechanism. To test this hypothesis, we let subjects (n = 4, macaque monkeys) view a large number of complex objects with consistently biased rewards with variable training durations (1, 5, or 30 + days). Following training, subjects searched for a high-value object (Good) among a variable number of low-value objects (Bad). Consistent with our hypothesis, we found that Good objects were accurately and quickly targeted, often by a single and direct saccade with a very short latency (<200 ms). The dependence of search times on display size reduced significantly with longer reward training, giving rise to a more efficient search (40 ms/item to 16 ms/item). This object-finding skill showed a large capacity for value-biased objects and was maintained in the long-term memory with no interference from reward learning with other objects. Such object-finding skill, and in particular its large capacity and long term retention, would be crucial for maximizing rewards and biological fitness throughout life where many objects are experienced continuously and/or intermittently.

[1]  M. Mishkin,et al.  Learning increases stimulus salience in anterior inferior temporal cortex of the macaque. , 2001, Journal of neurophysiology.

[2]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[3]  E. Reingold,et al.  Visual search asymmetry: The influence of stimulus familiarity and low-level features , 2001, Perception & psychophysics.

[4]  Patryk A. Laurent,et al.  Value-driven attentional capture , 2011, Proceedings of the National Academy of Sciences.

[5]  J. Theeuwes,et al.  Reward grabs the eye: Oculomotor capture by rewarding stimuli , 2012, Vision Research.

[6]  Hyoung F. Kim,et al.  Separate groups of dopamine neurons innervate caudate head and tail encoding flexible and stable value memories , 2014, Front. Neuroanat..

[7]  R. Shiffrin,et al.  Automatization and training in visual search. , 1992, The American journal of psychology.

[8]  Peter Dayan,et al.  Uncertainty and Learning , 2003 .

[9]  B. C. Motter,et al.  The zone of focal attention during active visual search , 1998, Vision Research.

[10]  M. Chun,et al.  Selecting and perceiving multiple visual objects , 2009, Trends in Cognitive Sciences.

[11]  Jacqueline Gottlieb,et al.  Neuronal Correlates of the Set-Size Effect in Monkey Lateral Intraparietal Area , 2008, PLoS biology.

[12]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[13]  C. Koch,et al.  A saliency-based search mechanism for overt and covert shifts of visual attention , 2000, Vision Research.

[14]  Ingo Rentschler,et al.  Loss of spatial phase relationships in extrafoveal vision , 1985, Nature.

[15]  Richard P. Heitz,et al.  Neural basis of the set-size effect in frontal eye field: timing of attention during visual search. , 2009, Journal of neurophysiology.

[16]  M. Chun,et al.  Contextual Cueing: Implicit Learning and Memory of Visual Context Guides Spatial Attention , 1998, Cognitive Psychology.

[17]  David L. Sheinberg,et al.  Distractor familiarity leads to more efficient visual search for complex stimuli , 2005, Perception & psychophysics.

[18]  P Cavanagh,et al.  Familiarity and pop-out in visual search , 1994, Perception & psychophysics.

[19]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[20]  J. Deniau,et al.  The lamellar organization of the rat substantia nigra pars reticulata: Distribution of projection neurons , 1992, Neuroscience.

[21]  Shinya Yamamoto,et al.  Reward Value-Contingent Changes of Visual Responses in the Primate Caudate Tail Associated with a Visuomotor Skill , 2013, The Journal of Neuroscience.

[22]  C. Gilbert,et al.  Learning to find a shape , 2000, Nature Neuroscience.

[23]  P. Strick,et al.  The temporal lobe is a target of output from the basal ganglia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. J. Brown,et al.  Peripheral visual acuity. , 1966, Archives of ophthalmology.

[25]  Yasushi Miyashita,et al.  Generation of fractal patterns for probing the visual memory , 1991, Neuroscience Research.

[26]  L. Chelazzi,et al.  Rewards teach visual selective attention , 2013, Vision Research.

[27]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

[28]  Ilya E. Monosov,et al.  What and Where Information in the Caudate Tail Guides Saccades to Visual Objects , 2012, The Journal of Neuroscience.

[29]  Hyoung F. Kim,et al.  Basal ganglia circuits for reward value-guided behavior. , 2014, Annual review of neuroscience.

[30]  Ali Ghazizadeh,et al.  Ecological Origins of Object Salience: Reward, Uncertainty, Aversiveness, and Novelty , 2016, Front. Neurosci..

[31]  Christof Koch,et al.  A Model of Saliency-Based Visual Attention for Rapid Scene Analysis , 2009 .

[32]  Walter Schneider,et al.  Controlled and automatic human information processing: II. Perceptual learning, automatic attending and a general theory. , 1977 .

[33]  O. Hikosaka,et al.  Robust Representation of Stable Object Values in the Oculomotor Basal Ganglia , 2012, The Journal of Neuroscience.

[34]  J. Wolfe,et al.  What attributes guide the deployment of visual attention and how do they do it? , 2004, Nature Reviews Neuroscience.

[35]  Hyoung F. Kim,et al.  Why skill matters , 2013, Trends in Cognitive Sciences.

[36]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[37]  I. Rentschler,et al.  Peripheral vision and pattern recognition: a review. , 2011, Journal of vision.

[38]  P. Goldman-Rakic,et al.  Organization of the nigrothalamocortical system in the rhesus monkey , 1985, The Journal of comparative neurology.

[39]  J. Wolfe,et al.  Preattentive Object Files: Shapeless Bundles of Basic Features , 1997, Vision Research.

[40]  Hyoung F. Kim,et al.  Distinct Basal Ganglia Circuits Controlling Behaviors Guided by Flexible and Stable Values , 2013, Neuron.

[41]  Robert M. McPeek,et al.  Concurrent processing of saccades in visual search , 2000, Vision Research.

[42]  Ali Ghazizadeh,et al.  Dopamine Neurons Encoding Long-Term Memory of Object Value for Habitual Behavior , 2015, Cell.

[43]  David L. Sheinberg,et al.  Eye movements during parallel-serial visual search. , 1997, Journal of experimental psychology. Human perception and performance.