Rhesus monkeys metacognitively monitor memories of the order of events

Human working memory is a capacity- and duration-limited system in which retention and manipulation of information is subject to metacognitive monitoring and control. At least some nonhuman animals appear to also monitor and control the contents of working memory, but only relatively simple cases where animals monitor or control the presence or absence of single memories have been studied. Here we combine a comparatively complex order memory task with methodology that assesses the capacity to introspect about memory. Monkeys observed sequential presentations of five images, and at test, reported which of two images from the list had appeared first during study. Concurrently, they chose to complete or avoid these tests on a trial-by-trial basis. Monkeys “knew when they knew” the correct response. They were less accurate discriminating images that had appeared close in time to one another during study and were more likely to avoid these difficult tests than they were to avoid easier tests. These results indicate that monkeys can metacognitively monitor relatively complex properties of the contents of working memory, including the quality of representations of temporal relations among images.

[1]  J. D. Smith,et al.  Animal metacognition: a tale of two comparative psychologies. , 2014, Journal of comparative psychology.

[2]  Elisabeth A. Murray,et al.  Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting , 2004, Animal Cognition.

[3]  Victoria L. Templer,et al.  Rats know when they remember: transfer of metacognitive responding across odor-based delayed match-to-sample tests , 2017, Animal Cognition.

[4]  Dissociation of item and source memory in rhesus monkeys , 2017, Cognition.

[5]  Victoria L. Templer,et al.  Cognitive mechanisms of memory for order in rhesus monkeys (Macaca mulatta) , 2013, Hippocampus.

[6]  Alessandra S. Souza,et al.  In search of the focus of attention in working memory: 13 years of the retro-cue effect , 2016, Attention, perception & psychophysics.

[7]  Victoria L. Templer,et al.  An assessment of domain-general metacognitive responding in rhesus monkeys , 2017, Behavioural Processes.

[8]  H. Eichenbaum,et al.  Memory for the Order of Events in Specific Sequences: Contributions of the Hippocampus and Medial Prefrontal Cortex , 2011, The Journal of Neuroscience.

[9]  A. Reber Implicit learning and tacit knowledge , 1993 .

[10]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[11]  Mathieu Wolff,et al.  Beyond Spatial Memory: The Anterior Thalamus and Memory for the Temporal Order of a Sequence of Odor Cues , 2006, The Journal of Neuroscience.

[12]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[13]  Guenter Corssen,et al.  Alcohol‐Induced Pituitary Adenolysis: How Does It Control Intractable Cancer Pain?—An Experimental Study Using Tooth Pulp‐Evoked Potentials in Rhesus Monkeys , 1979 .

[14]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[15]  Claudia M. Roebers,et al.  Executive function and metacognition: Towards a unifying framework of cognitive self-regulation , 2017 .

[16]  Victoria L. Templer,et al.  Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests , 2012, Animal Cognition.

[17]  Norbert J. Fortin,et al.  The evolution of episodic memory , 2013, Proceedings of the National Academy of Sciences.

[18]  R. Hampton Rhesus monkeys know when they remember , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[19]  J. D. Smith,et al.  Primate cognition: attention, episodic memory, prospective memory, self-control, and metacognition as examples of cognitive control in nonhuman primates. , 2016, Wiley interdisciplinary reviews. Cognitive science.

[20]  Robert R Hampton,et al.  Multiple demonstrations of metacognition in nonhumans: Converging evidence or multiple mechanisms? , 2009, Comparative cognition & behavior reviews.

[21]  J. D. Smith,et al.  Executive-attentional uncertainty responses by rhesus macaques (Macaca mulatta). , 2013, Journal of experimental psychology. General.

[22]  Seth J. Ramus,et al.  Intact Artificial Grammar Learning in Amnesia: Dissociation of Classification Learning and Explicit Memory for Specific Instances , 1992 .

[23]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

[24]  Robert R. Hampton,et al.  Dissociation of active working memory and passive recognition in rhesus monkeys , 2013, Cognition.

[25]  J. D. Smith,et al.  Memory monitoring by animals and humans. , 1998, Journal of experimental psychology. General.

[26]  L. Jarrard,et al.  Contributions of the hippocampus and medial prefrontal cortex to energy and body weight regulation , 2009, Hippocampus.

[27]  Victoria L. Templer,et al.  Journal of Experimental Psychology: General Evaluation of Seven Hypotheses for Metamemory Performance in Rhesus Monkeys , 2014 .

[28]  R. Hampton,et al.  Rhesus monkeys (Macaca mulatta) adaptively adjust information seeking in response to information accumulated. , 2015, Journal of comparative psychology.

[29]  R. Hampton,et al.  Thatcher Effect in Monkeys Demonstrates Conservation of Face Perception across Primates , 2009, Current Biology.

[30]  H. Terrace,et al.  The Missing Link in Cognition: Origins of Self-Reflective Consciousness , 2005 .

[31]  T. O. Nelson Consciousness and metacognition. , 1996 .

[32]  J. Hodges Memory, Amnesia and the Hippocampal System , 1995 .

[33]  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.

[34]  Paul E. Gilbert,et al.  The role of the hippocampus in memory for the temporal order of a sequence of odors. , 2002, Behavioral neuroscience.

[35]  D. Schacter,et al.  The Evolution of Multiple Memory Systems , 1987 .

[36]  K. Jellinger,et al.  The Missing Link in Cognition. Origins of self-reflective consciousness , 2009 .

[37]  K. Oberauer,et al.  Attention to Information in Working Memory , 2012 .

[38]  Matthew L Shapiro,et al.  Memory Time , 2011, Neuron.

[39]  J. D. Smith,et al.  Confidence judgments by humans and rhesus monkeys. , 2005, The Journal of general psychology.

[40]  G. Winocur,et al.  Episodic Memory and Beyond: The Hippocampus and Neocortex in Transformation. , 2016, Annual review of psychology.

[41]  R. Engle,et al.  The nature of individual differences in working memory capacity: active maintenance in primary memory and controlled search from secondary memory. , 2007, Psychological review.

[42]  R. Hampton,et al.  Control of working memory in rhesus monkeys (Macaca mulatta). , 2014, Journal of experimental psychology. Animal learning and cognition.