What does preferential viewing tell us about the neurobiology of recognition memory?

The two tests most widely used in nonhuman primates to assess the neurobiology of recognition memory produce conflicting results. Preferential viewing tests (e.g.

Motor System-Dependent Effects of Amygdala and Ventral Striatum Lesions on Explore-Exploit Behaviors.

Deciding whether to forego immediate rewards or explore new opportunities is a key component of flexible behavior and is critical for the survival of the species. Although previous studies have shown that different cortical and subcortical areas, including the amygdala and ventral striatum (VS), are implicated in representing the immediate (exploitative) and future (explorative) value of choices, the effect of the motor system used to make choices has not been examined. Here, we tested male rhesus macaques with amygdala or VS lesions on two versions of a three-arm bandit task where choices were registered with either a saccade or an arm movement.

The amygdala is not necessary for the familiarity aspect of recognition memory.

Dual-process accounts of item recognition posit two memory processes: slow but detailed recollection, and quick but vague familiarity. It has been proposed, based on prior rodent work, that the amygdala is critical for the familiarity aspect of item recognition. Here, we evaluated this proposal in male rhesus monkeys (Macaca mulatta) with selective bilateral excitotoxic amygdala damage.

Interspecific differences in the effects of masking and distraction on anti-predator behavior in suburban anthropogenic noise.

Predation is a common threat to animal survival. The detection of predators or anti-predator communication signals can be disrupted by anthropogenic noise; however, the mechanism by which responses are affected is unclear. Masking and distraction are the two hypotheses that have emerged as likely explanations for changes in behavior in noise.

Reevaluating the role of the hippocampus in memory: A meta-analysis of neurotoxic lesion studies in nonhuman primates.

The hippocampus and perirhinal cortex are both broadly implicated in memory; nevertheless, their relative contributions to visual item recognition and location memory remain disputed. Neuropsychological studies in nonhuman primates that examine memory function after selective damage to medial temporal lobe structures report various levels of memory impairment-ranging from minor deficits to profound amnesia. The discrepancies in published findings have complicated efforts to determine the exact magnitude of visual item recognition and location memory impairments following damage to the hippocampus and/or perirhinal cortex.

Autonomic arousal tracks outcome salience not valence in monkeys making social decisions.

The evolutionary and neural underpinnings of human prosociality are still being identified. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, called vicarious reinforcement, and that this capacity is supported by a network of brain areas including the anterior cingulate cortex (ACC) and the amygdala. At the same time, analyses of autonomic arousal have been increasingly used to contextualize and guide neural research, especially for studies of reward processing.

No evidence that monkeys attribute mental states to animated shapes in the Heider-Simmel videos.

Human Theory of Mind (ToM) is so automatic and pervasive that we spontaneously attribute mental states to animated abstract shapes, as evidenced by the classic Heider-Simmel findings. The extent to which this represents a fundamental characteristic of primate social cognition is debated. Prior research suggests that monkeys spontaneously predict behavior and attribute basic goals to conspecifics, but it remains unclear whether, like humans, they spontaneously ascribe mental states to animated shapes.

Effects of Amygdala Lesions on Object-Based Versus Action-Based Learning in Macaques.

The neural systems that underlie reinforcement learning (RL) allow animals to adapt to changes in their environment. In the present study, we examined the hypothesis that the amygdala would have a preferential role in learning the values of visual objects. We compared a group of monkeys (Macaca mulatta) with amygdala lesions to a group of unoperated controls on a two-armed bandit reversal learning task.

Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions.

The theory that the hippocampus is critical for visual memory and relational cognition has been challenged by discovery of more spared hippocampal tissue than previously reported in H.M., previously unreported extra-hippocampal damage in developmental amnesiacs, and findings that the hippocampus is unnecessary for object-in-context memory in monkeys.

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys.

A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey.

Hippocampal damage attenuates habituation to videos in monkeys.

Monkeys with selective damage to the hippocampus are often unimpaired in matching-to-sample tests but are reportedly impaired in visual paired comparison. While both tests assess recognition of previously seen images, delayed matching-to-sample may engage active memory maintenance whereas visual paired comparison may not. Passive memory tests that are not rewarded with food and that do not require extensive training may provide more sensitive measures of hippocampal function.

Dissociation of memory signals for metamemory in rhesus monkeys (Macaca mulatta).

Some nonhuman species demonstrate metamemory, the ability to monitor and control memory. Here, we identify memory signals that control metamemory judgments in rhesus monkeys by directly comparing performance in two metamemory paradigms while holding the availability of one memory signal constant and manipulating another. Monkeys performed a four-choice match-to-sample memory task.

Nonnavigational spatial memory performance is unaffected by hippocampal damage in monkeys.

Evidence that the hippocampus is critical for spatial memory in nonnavigational tests is mixed. A recent study reported that temporary hippocampal inactivation impaired spatial memory in the nonnavigational Hamilton Search Task in monkeys. However, several studies have documented no impairment on other nonnavigational spatial memory tests following permanent hippocampal lesions.

Amygdala lesions eliminate viewing preferences for faces in rhesus monkeys.

In free-viewing experiments, primates orient preferentially toward faces and face-like stimuli. To investigate the neural basis of this behavior, we measured the spontaneous viewing preferences of monkeys with selective bilateral amygdala lesions. The results revealed that when faces and nonface objects were presented simultaneously, monkeys with amygdala lesions had no viewing preference for either conspecific faces or illusory facial features in everyday objects.

MRI Overestimates Excitotoxic Amygdala Lesion Damage in Rhesus Monkeys.

Selective, fiber-sparing excitotoxic lesions are a state-of-the-art tool for determining the causal contributions of different brain areas to behavior. For nonhuman primates especially, it is advantageous to keep subjects with high-quality lesions alive and contributing to science for many years. However, this requires the ability to estimate lesion extent accurately.

Dissociation of item and source memory in rhesus monkeys.

Source memory, or memory for the context in which a memory was formed, is a defining characteristic of human episodic memory and source memory errors are a debilitating symptom of memory dysfunction. Evidence for source memory in nonhuman primates is sparse despite considerable evidence for other types of sophisticated memory and the practical need for good models of episodic memory in nonhuman primates. A previous study showed that rhesus monkeys confused the identity of a monkey they saw with a monkey they heard, but only after an extended memory delay.

Specialized areas for value updating and goal selection in the primate orbitofrontal cortex.

The macaque orbitofrontal cortex (OFC) is essential for selecting goals based on current, updated values of expected reward outcomes. As monkeys consume a given type of reward to satiety, its value diminishes, and OFC damage impairs the ability to shift goal choices away from devalued outcomes. To examine the contributions of OFC's components to goal selection, we reversibly inactivated either its anterior (area 11) or posterior (area 13) parts.

Similar stimulus features control visual classification in orangutans and rhesus monkeys.

Many species classify images according to visual attributes. In pigeons, local features may disproportionately control classification, whereas in primates global features may exert greater control. In the absence of explicitly comparative studies, in which different species are tested with the same stimuli under similar conditions, it is not possible to determine how much of the variation in the control of classification is due to species differences and how much is due to differences in the stimuli, training, or testing conditions.

Two-item same/different discrimination in rhesus monkeys (Macaca mulatta).

Almost all nonhuman animals can recognize when one item is the same as another item. It is less clear whether nonhuman animals possess abstract concepts of "same" and "different" that can be divorced from perceptual similarity. Pigeons and monkeys show inconsistent performance, and often surprising difficulty, in laboratory tests of same/different learning that involve only two items.

Evaluation of seven hypotheses for metamemory performance in rhesus monkeys.

Knowing the extent to which nonhumans and humans share mechanisms for metacognition will advance our understanding of cognitive evolution and will improve selection of model systems for biomedical research. Some nonhuman species avoid difficult cognitive tests, seek information when ignorant, or otherwise behave in ways consistent with metacognition. There is agreement that some nonhuman animals "succeed" in these metacognitive tasks, but little consensus about the cognitive mechanisms underlying performance.

Metacognition as discrimination: commentary on Smith et al. (2014).

Smith, Couchman, and Beran (2014, pp. 115-131) critique recent "low-level" associative process models of nonhuman metacognition. We agree with many aspects of their critique.

Dissociation of visual localization and visual detection in rhesus monkeys (Macaca mulatta).

Conscious and unconscious cognitive processes contribute independently to human behavior and can be dissociated. For example, humans report failing to see objects clearly in the periphery while simultaneously being able to grasp those objects accurately (Milner in Proc R Soc B Biol Sci 279:2289-2298, 2012). Knowing whether similar dissociations are present in nonverbal species is critical to our understanding of comparative psychology and the evolution of brains.

Recognition errors suggest fast familiarity and slow recollection in rhesus monkeys.

One influential model of recognition posits two underlying memory processes: recollection, which is detailed but relatively slow, and familiarity, which is quick but lacks detail. Most of the evidence for this dual-process model in nonhumans has come from analyses of receiver operating characteristic (ROC) curves in rats, but whether ROC analyses can demonstrate dual processes has been repeatedly challenged. Here, we present independent converging evidence for the dual-process model from analyses of recognition errors made by rhesus monkeys.

Dissociation of active working memory and passive recognition in rhesus monkeys.

Active cognitive control of working memory is central in most human memory models, but behavioral evidence for such control in nonhuman primates is absent and neurophysiological evidence, while suggestive, is indirect. We present behavioral evidence that monkey memory for familiar images is under active cognitive control. Concurrent cognitive demands during the memory delay impaired matching-to-sample performance for familiar images in a demand-dependent manner, indicating that maintaining these images in memory taxed limited cognitive resources.