Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests

Abstract

The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton, 2001; Smith, Shields, & Washburn, 2003). (R.R. Hampton, 2001; Smith, Shields, & Washburn, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.

Assessment of metacognitive monitoring and control in baboons (Papio papio)

“…The third test manipulated the stimulus brightness and stimulus duration simultaneously in order to change task difficulty. The aim of the Test 3 was to control for novelty effects and to confirm that the use of the Repeat key really depended on the difficulty of the trial (Templer and Hampton 2012).…”

Not knowing what one knows: A Meaningful failure of metacognition in capuchin monkeys.

“…Yet again, humans ( Figure 2A) and monkeys ( Figure 2B) displayed an increase in the use of the UR corresponding with a decrease in use of the categorization responses for the most difficult trials. Other experiments explored metacognition in rhesus monkeys and showed that the use of the UR or other metacognitive responses transfers across a variety of different tasks (Basile, Schroeder, Brown, Templer, & Hampton, 2015;Brown, Templer, & Hampton, 2017;Kornell, Son, & Terrace, 2007;Smith, Redford, Beran, & Washburn, 2010;Templer & Hampton, 2012) and that monkeys will continue using the UR when feedback is delayed (Smith, Beran, Redford, & Washburn, 2006), minimizing the likelihood that task-specific environmental cues are responsible for the use of the UR. Figure 1. A.…”

“…Thus, the macaques reported uncertainty in their recall under conditions in which no single environmental stimulus could easily cue the UR response and when the likelihood of correctly responding on the task was small. Templer and Hampton (2012) also presented rhesus monkeys with a set of memory tasks and found that the monkeys were consistently more accurate on trials where they could have avoided answering the primary question than on trials where they were forced to answer it. And, the monkeys adjusted their use of trial declining responses depending on whether the various tasks made it easier or harder to remember stimuli.…”

Go when you know: Chimpanzees’ confidence movements reflect their responses in a computerized memory task

“…Animals cannot easily report their confidence in these ways. However, rhesus monkeys and rats can provide other responses that reflect the monitoring of uncertainty of their perceptual experiences (Beran, Smith, Redford, & Washburn, 2006; Foote & Crystal, 2007, 2012; Shields, Smith, & Washburn, 1997; Smith, Beran, Redford, & Washburn, 2006; Smith, Redford, Beran, & Washburn, 2010; Smith, Schull, Strote, McGee, Egnor, & Erb, 1995; Smith, Shields, Schull, & Washburn, 1997) and pigeons, rhesus monkeys, and orangutans provide responses that reflect monitoring of memory (Adams & Santi, 2011; Basile, Hampton, Suomi, & Murray, 2009; Fujita, 2009; Hampton, 2001; Hampton & Hampstead, 2006; Inman & Shettleworth, 1999; Smith, Shields, Allendoerfer, & Washburn, 1998; Suda-King, 2008; Suda-King, Bania, Stromberg, & Subiaul, 2013; Sutton & Shettleworth, 2008; Templer & Hampton, 2012). Rhesus monkeys, chimpanzees, orangutans, and pigeons have demonstrated the ability to search for needed information (Beran & Smith, 2011; Beran, Smith, & Perdue, 2013; Call, 2010; Call & Carpenter, 2001; Castro & Wasserman, 2013; Hampton, Zivin, & Murray, 2004; Iwasaki, Watanabe, & Fujita, 2013; Kirk, McMillan, & Roberts, 2014; Marsh & MacDonald, 2012a, 2012b; Roberts et al, 2009), and have even shown the capacity to make confidence judgments about the outcomes of already completed responses, although only with extensive training (Kornell, Son, & Terrace, 2007; Morgan, Kornell, Kornblum, & Terrace, 2014; Nakamura, Watanabe, Betsuyaku, & Fujita, 2011; Shields, Smith, Guttmannova, & Washburn, 2005).…”