Automatic comparison of stimulus durations in the primate prefrontal cortex: the neural basis of across-task interference.

Rhesus monkeys performed two tasks, both requiring a choice between a red square and a blue circle. In the duration task, the two stimuli appeared sequentially on each trial, for varying durations, and, later, during the choice phase of the task, the monkeys needed to choose the one that had lasted longer. In the matching-to-sample task, one of the two stimuli appeared twice as a sample, with durations matching those in the duration task, and the monkey needed to choose that stimulus during the choice phase. Although stimulus duration was irrelevant in the matching-to-sample task, the monkeys made twice as many errors when the second stimulus was shorter. This across-task interference supports an order-dependent model of the monkeys' choice and reveals something about their strategy in the duration task. The monkeys tended to choose the second stimulus when its duration exceeded the first and to choose the alternative stimulus otherwise. For the duration task, this strategy obviated the need to store stimulus-duration conjunctions for both stimuli, but it generated errors on the matching-to-sample task. We examined duration coding in prefrontal neurons and confirmed that a population of cells encoded relative duration during the matching-to-sample task, as expected from the order-dependent errors.

[1]  Samir Tamer,et al.  Target Detection , 2009, Encyclopedia of Biometrics.

[2]  J. Duncan The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[3]  Aldo Genovesio,et al.  The influence of recent decisions on future goal selection , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  J. Tanji,et al.  Behavioral planning in the prefrontal cortex , 2001, Current Opinion in Neurobiology.

[5]  Aldo Genovesio,et al.  Encoding Goals but Not Abstract Magnitude in the Primate Prefrontal Cortex , 2012, Neuron.

[6]  J. Tanji,et al.  Neuronal activity in the primate prefrontal cortex in the process of motor selection based on two behavioral rules. , 2000, Journal of neurophysiology.

[7]  Ventral premotor cortex neuronal activity matches perceptual decisions , 2011, The European journal of neuroscience.

[8]  Aldo Genovesio,et al.  Feature- and Order-Based Timing Representations in the Frontal Cortex , 2009, Neuron.

[9]  S. Wise,et al.  Neuronal activity related to elapsed time in prefrontal cortex. , 2006, Journal of neurophysiology.

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

[11]  J. Martinez-Trujillo,et al.  Strength of Response Suppression to Distracter Stimuli Determines Attentional-Filtering Performance in Primate Prefrontal Neurons , 2011, Neuron.

[12]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[13]  Daeyeol Lee,et al.  Prefrontal Coding of Temporally Discounted Values during Intertemporal Choice , 2008, Neuron.

[14]  Earl K Miller,et al.  The representation of multiple objects in prefrontal neuronal delay activity. , 2007, Cerebral cortex.

[15]  Aldo Genovesio,et al.  Prefrontal–parietal function: from foraging to foresight , 2014, Trends in Cognitive Sciences.

[16]  S. Funahashi,et al.  Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation , 1997, Behavioural Brain Research.

[17]  Masaki Tanaka,et al.  Neuronal Correlates of Multiple Top–Down Signals during Covert Tracking of Moving Objects in Macaque Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

[18]  Tatiana Pasternak,et al.  Flexibility of Sensory Representations in Prefrontal Cortex Depends on Cell Type , 2009, Neuron.

[19]  P. Goldman-Rakic,et al.  Comparison of human infants and rhesus monkeys on Piaget's AB task: evidence for dependence on dorsolateral prefrontal cortex , 2004, Experimental Brain Research.

[20]  J. Tanji,et al.  Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. , 2003, Journal of neurophysiology.

[21]  Tatiana Pasternak,et al.  Memory-Guided Sensory Comparisons in the Prefrontal Cortex: Contribution of Putative Pyramidal Cells and Interneurons , 2012, The Journal of Neuroscience.

[22]  G. Woodman,et al.  Do the contents of visual working memory automatically influence attentional selection during visual search? , 2007, Journal of experimental psychology. Human perception and performance.

[23]  Michael E. Goldberg,et al.  Prefrontal Neurons Coding Suppression of Specific Saccades , 2004, Neuron.

[24]  Andreas Nieder,et al.  Contributions of primate prefrontal and posterior parietal cortices to length and numerosity representation. , 2009, Journal of neurophysiology.

[25]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[26]  John Duncan,et al.  Target Detection by Opponent Coding in Monkey Prefrontal Cortex , 2010, Journal of Cognitive Neuroscience.

[27]  Aldo Genovesio,et al.  Prefrontal Cortex Activity during the Discrimination of Relative Distance , 2011, The Journal of Neuroscience.

[28]  P. H. Schiller,et al.  Conditional task-related responses in monkey dorsomedial frontal cortex , 2004, Experimental Brain Research.

[29]  A Genovesio,et al.  From duration and distance comparisons to goal encoding in prefrontal cortex. , 2014, Advances in experimental medicine and biology.

[30]  B. Milner,et al.  Frontal lobes and the temporal organization of memory. , 1985, Human neurobiology.

[31]  Daeyeol Lee,et al.  Activity in prefrontal cortex during dynamic selection of action sequences , 2006, Nature Neuroscience.

[32]  M. Petrides Functional specialization within the dorsolateral frontal cortex for serial order memory , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  O. Hikosaka,et al.  Responses to task-irrelevant visual features by primate prefrontal neurons. , 2001, Journal of neurophysiology.

[34]  R. Goebel,et al.  Task-Relevant and Accessory Items in Working Memory Have Opposite Effects on Activity in Extrastriate Cortex , 2012, The Journal of Neuroscience.

[35]  The neurophysiology of abstract response strategies , 2007 .

[36]  J. Tanji,et al.  Integration of temporal order and object information in the monkey lateral prefrontal cortex. , 2004, Journal of neurophysiology.

[37]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[38]  Christos Constantinidis,et al.  Neural Correlates of a Decision Variable Before Learning to Perform a Match/Non-Match Task , 2012, The Journal of Neuroscience.

[39]  Aldo Genovesio,et al.  Representation of Future and Previous Spatial Goals by Separate Neural Populations in Prefrontal Cortex , 2006, The Journal of Neuroscience.

[40]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[41]  Bradley R. Postle,et al.  The Prefrontal Cortex and Oculomotor Delayed Response: A Reconsideration of the “Mnemonic Scotoma” , 2012, Journal of Cognitive Neuroscience.

[42]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[43]  Andrew R. Mitz,et al.  MatOFF: A tool for analyzing behaviorally complex neurophysiological experiments , 2007, Journal of Neuroscience Methods.

[44]  S. Wise,et al.  Autonomous Encoding of Irrelevant Goals and Outcomes by Prefrontal Cortex Neurons , 2014, The Journal of Neuroscience.

[45]  Steven P. Wise,et al.  Neuronal activity in dorsomedial frontal cortex and prefrontal cortex reflecting irrelevant stimulus dimensions , 2001, Experimental Brain Research.

[46]  S. Wise,et al.  Neuronal Activity during a Cued Strategy Task: Comparison of Dorsolateral, Orbital, and Polar Prefrontal Cortex , 2012, The Journal of Neuroscience.