Ecological Origins of Object Salience: Reward, Uncertainty, Aversiveness, and Novelty

Among many objects around us, some are more salient than others (i.e., attract our attention automatically). Some objects may be inherently salient (e.g., brighter), while others may become salient by virtue of their ecological relevance through experience. However, the role of ecological experience in automatic attention has not been studied systematically. To address this question, we let subjects (macaque monkeys) view a large number of complex objects (>300), each experienced repeatedly (>5 days) with rewarding, aversive or no outcome association (mere-perceptual exposure). Test of salience was done on separate days using free viewing with no outcome. We found that gaze was biased among the objects from the outset, affecting saccades to objects or fixations within objects. When the outcome was rewarding, gaze preference was stronger (i.e., positive) for objects with larger or equal but uncertain rewards. The effects of aversive outcomes were variable. Gaze preference was positive for some outcome associations (e.g., airpuff), but negative for others (e.g., time-out), possibly due to differences in threat levels. Finally, novel objects attracted gaze, but mere perceptual exposure of objects reduced their salience (learned negative salience). Our results show that, in primates, object salience is strongly influenced by previous ecological experience and is supported by a large memory capacity. Owing to such high capacity for learned salience, the ability to rapidly choose important objects can grow during the entire life to promote biological fitness.

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

[2]  Karin Mogg,et al.  Covert and overt orienting of attention to emotional faces in anxiety , 2000 .

[3]  Ingmar H. A. Franken,et al.  Differences in attention to food and food intake between overweight/obese and normal-weight females under conditions of hunger and satiety , 2010, Appetite.

[4]  Benjamin Y. Hayden,et al.  Temporal Discounting Predicts Risk Sensitivity in Rhesus Macaques , 2007, Current Biology.

[5]  M. W. Brown,et al.  Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex , 2004, Experimental Brain Research.

[6]  G. Zelinsky,et al.  A new look at novelty effects: Guiding search away from old distractors , 2009, Attention, perception & psychophysics.

[7]  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.

[8]  Okihide Hikosaka,et al.  Selective and graded coding of reward uncertainty by neurons in the primate anterodorsal septal region , 2013, Nature Neuroscience.

[9]  Michael S. Gaffrey,et al.  Stimulus-Driven Attention, Threat Bias, and Sad Bias in Youth with a History of an Anxiety Disorder or Depression , 2016, Journal of abnormal child psychology.

[10]  T. Robinson The neural basis of drug craving : an ~ ~ ~ ~ ~ tive ~ sensiti ~ atiun theory of addiction , 2002 .

[11]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

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

[13]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[14]  Shaul Hochstein,et al.  At first sight: A high-level pop out effect for faces , 2005, Vision Research.

[15]  J. Theeuwes,et al.  Attentional prioritisation of threatening information: Examining the role of the size of the attentional window , 2013, Cognition & emotion.

[16]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[17]  J. Theeuwes,et al.  Faces capture attention: Evidence from inhibition of return , 2006 .

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

[19]  R. Zajonc Attitudinal effects of mere exposure. , 1968 .

[20]  M. Just,et al.  Eye fixations and cognitive processes , 1976, Cognitive Psychology.

[21]  M. Balaban,et al.  Salience of fear/threat in the affective modulation of the human startle blink , 1994, Biological Psychology.

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

[23]  K. Mogg,et al.  Orienting of Attention to Threatening Facial Expressions Presented under Conditions of Restricted Awareness , 1999 .

[24]  L. Chelazzi,et al.  Learning to Attend and to Ignore Is a Matter of Gains and Losses , 2009, Psychological science.

[25]  H. Collewijn,et al.  Human eye movements associated with blinks and prolonged eyelid closure. , 1985, Journal of neurophysiology.

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

[27]  Shinsuke Shimojo,et al.  Roles of familiarity and novelty in visual preference judgments are segregated across object categories , 2009, Proceedings of the National Academy of Sciences.

[28]  Sara E. Morrison,et al.  Representations of appetitive and aversive information in the primate orbitofrontal cortex , 2011, Annals of the New York Academy of Sciences.

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

[30]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[31]  Chad J Marsolek,et al.  What form of memory underlies novelty preferences? , 2008, Psychonomic bulletin & review.

[32]  M. Platt,et al.  Risk-sensitive neurons in macaque posterior cingulate cortex , 2005, Nature Neuroscience.

[33]  D. Berlyne Novelty, complexity, and hedonic value , 1970 .

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

[35]  C. Olson,et al.  In Monkeys Making Value-Based Decisions, LIP Neurons Encode Cue Salience and Not Action Value , 2012, Science.

[36]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[37]  Lester C. Loschky,et al.  The limits of visual resolution in natural scene viewing , 2005 .

[38]  W. Schultz,et al.  Coding of Reward Risk by Orbitofrontal Neurons Is Mostly Distinct from Coding of Reward Value , 2010, Neuron.

[39]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[40]  W. Johnston,et al.  Attention capture by novel stimuli. , 1990, Journal of experimental psychology. General.

[41]  E. Rolls,et al.  The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks , 2004, Experimental Brain Research.

[42]  O. Hikosaka The habenula: from stress evasion to value-based decision-making , 2010, Nature Reviews Neuroscience.

[43]  Christopher J. Peck,et al.  Reward Modulates Attention Independently of Action Value in Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[44]  Jan Theeuwes,et al.  Attentional capture by signals of threat , 2014, Cognition & emotion.

[45]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[46]  William R. Stauffer,et al.  Dopamine Reward Prediction Error Responses Reflect Marginal Utility , 2014, Current Biology.

[47]  R. L. Fantz Visual Experience in Infants: Decreased Attention to Familiar Patterns Relative to Novel Ones , 1964, Science.

[48]  Minryung R. Song,et al.  Multiphasic Temporal Dynamics in Responses of Midbrain Dopamine Neurons to Appetitive and Aversive Stimuli , 2013, The Journal of Neuroscience.

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

[50]  Denise Manahan-Vaughan,et al.  Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[51]  M. Mishkin,et al.  Stimulus recognition , 1994, Current Opinion in Neurobiology.

[52]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

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

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

[55]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[56]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[57]  W. Runquist,et al.  The relation between physiological measures of emotionality and performance in eyelid conditioning. , 1959, Journal of experimental psychology.

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

[59]  Gretchen Kambe,et al.  Detection of Differential Viewing Patterns to Erotic and Non-Erotic Stimuli Using Eye-Tracking Methodology , 2006, Archives of sexual behavior.

[60]  J. Russell A circumplex model of affect. , 1980 .

[61]  Hiroshi Yamada,et al.  Thirst-dependent risk preferences in monkeys identify a primitive form of wealth , 2013, Proceedings of the National Academy of Sciences.

[62]  T. Nakada,et al.  A Review of EEG and Blood Flow Data , 1998, Reviews in the neurosciences.

[63]  D. Gaffan,et al.  Impaired Recency Judgments and Intact Novelty Judgments after Fornix Transection in Monkeys , 2004, Journal of Neuroscience.

[64]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[65]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

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

[67]  N. Azrin,et al.  Attack, avoidance, and escape reactions to aversive shock. , 1967, Journal of the experimental analysis of behavior.

[68]  Elizabeth A Buffalo,et al.  Recognition memory signals in the macaque hippocampus , 2009, Proceedings of the National Academy of Sciences.

[69]  A J Van Opstal,et al.  Blink-perturbed saccades in monkey. I. Behavioral analysis. , 2000, Journal of neurophysiology.