Adaptive memory: fitness relevant stimuli show a memory advantage in a game of pelmanism

A pelmanism (matched-pairs) game was used in order to test the hypothesis that survival-relevant stimuli that are likely to have been present during human evolution (e.g., a snake in attack position) enjoy a memory advantage over other survival-relevant (but “modern”) stimuli (e.g., a threatening image of a gunman). Survival-relevant stimuli were matched for arousal and presented in one of two 5 x 4 grids, along with filler items. Participants were asked to match the pairs in the grids by clicking on successive squares to reveal stimuli. Participants made significantly fewer errors when matching evolutionarily relevant survival stimuli than when matching the other stimuli. Additionally, on incorrect trials, the attempted matches were significantly closer to the actual locations of evolutionarily relevant targets than to those of other stimuli. The results suggest that objects that likely posed a consistent threat throughout human evolutionary history are better remembered than other, equally arousing and survival-relevant, stimuli. [corrected]     

Long-term memory of color stimuli in the jungle crow (Corvus macrorhynchos)

Wild-caught jungle crows (n = 20) were trained to discriminate between color stimuli in a two-alternative discrimination task. Next, crows were tested for long-term memory after 1-, 2-, 3-, 6-, and 10-month retention intervals. This preliminary study showed that jungle crows learn the task and reach a discrimination criterion (80% or more correct choices in two consecutive sessions of ten trials) in a few trials, and some even in a single session. Most, if not all, crows successfully remembered the constantly reinforced visual stimulus during training after all retention intervals. These results suggest that jungle crows have a high retention capacity for learned information, at least after a 10-month retention interval and make no or very few errors. This study is the first to show long-term memory capacity of color stimuli in corvids following a brief training that memory rather than rehearsal was apparent. Memory of visual color information is vital for exploitation of biological resources in crows. We suspect that jungle crows could remember the learned color discrimination task even after a much longer retention interval.     

Immediate memory and simultaneous stimuli

When two sets of digits are presented simultaneously one to one ear and one to the other, the subject may be asked to write them down from immediate memory beginning with those on an ear chosen by the experimenter. He can do this, but any mistakes are usually amongst those on the ear prescribed for later response. If the subject does not know the order of recall until after stimulation, he either shows low efficiency with the same serial order effect, or else normal efficiency with an altered serial order effect.

When the order of recall is known in advance, efficiency is also reduced by altering the time of presentation of the last items to be recalled; and also by inserting irrelevant items. All these facts are consistent with a particular theory of immediate memory.     

Facial reactions to different emotionally relevant stimuli

Facial EMG activity was measured from the Corrugator supercilii and the Zygomatic major muscle regions while 48 subjects were exposed to pictures of angry and happy facial expressions, snakes and flowers as well as low and high preference nature scenes. The valency perspective predicted that facial reactions should be related to the intensity of the positive and the negative valency of stimuli. The mimicking behavior approach predicted that facial reactions should only be reflected as a mimicking response to the facial stimuli, whereas the evolutionary:biological perspective predicted that the most clearcut positive and negative facial reactions should be evoked by facial stimuli and by snakes. In support of the latter perspective, the present results showed that angry faces and snakes evoked the most distinct Corrugator supercilii muscle response, whereas happy faces evoked the largest Zygomatic major muscle response.     

Eye color and responsiveness to arousing stimuli.

The hypothesis was advanced that dark-eyed subjects are more responsive to arousing stimuli than light-eyed subjects. 40 subjects listened to neutral and arousing auditory stimuli and viewed scenes which were neutral, violent, or sexual in nature. The dependent measure of arousal was a score derived from a combination of physiological responses recorded on a polygraph. Scores were significantly higher for dark-eyed than light-eyed subjects. Significant sex differences were also found, females having higher scores than males. Implications for future research and application were discussed.     

Shifting human color memory

Persons who witnessed an automobile accident involving a green car were exposed to information that the car was blue. On a subsequent color recognition test, most subjects shifted their color selection in the direction of the misleading information and away from the actual perceived color. Shifting was greater for subjects who did not initially commit themselves to a color selection. Control subjects, who were not exposed to misleading information, distributed their chokes around the true color, and did not show a systematic color shift over time.     

Encoding and memory for verbal and pictorial stimuli

Memory for visually presented verbal and pictorial material was compared using stimuli chosen to minimize non-essential differences between the two types of material. Experiment I required retention of a short list; verbal and pictorial stimuli were remembered equally well. Experiment II required recall of single items after 30 s of backwards counting; recall was much superior for pictorial stimuli. The type of task appeared to affect encoding, with verbal encoding reported to be predominant in Experiment I and visual encoding, or imagery, common in Experiment II.     

Emotional stimuli, divided attention, and memory

The emotion-memory literature has shown that negative emotional arousal enhances memory. S. A. Christianson (1992) proposed that preattentive processing could account for this emotion-memory relationship. Two experiments were conducted to test Christianson's theory. In Experiment 1, participants were exposed to neutral and negative arousing slides. In Experiment 2, participants were exposed to neutral, negative arousing, and positive arousing slides. In both experiments, the aforementioned variable was factorially combined with a divided-attention or non-divided-attention condition. The authors predicted that, in contrast to the nondivided condition, dividing attention would adversely impact neutral and positive stimuli more than negative stimuli. The hypothesis was supported; participants recalled more high negative-arousal slides than positive or neutral slides when their attention was divided rather than nondivided.     

Stress affects the selection of relevant from irrelevant stimuli

Two experiments were used to examine the effects of stress on latent inhibition (LI; poorer learning with a previously exposed irrelevant stimulus rather than a novel stimulus). In Experiment 1, stress was induced in college students by threatening participants' self-esteem with a difficult number series completion test that was related to intelligence. In Experiment 2, the participants were job seekers who were either informed or not that the LI test was part of the selection process. In both experiments, LI was attenuated in high- as compared with low-stressed participants. The results suggest that stress and/or anxiety impairs the inhibition of irrelevant-preexposed stimuli. Implications for understanding the impaired selective attentional processes in schizophrenia and schizotypy are discussed.     

Synesthetic color experiences influence memory

We describe the extraordinary memory of C, a 21–year–old student who experiences synesthetic colors (i.e., photisms) when she sees, hears, or thinks of digits. Using three matrices of 50 digits, we tested C and 7 nonsynesthetes to evaluate whether C's synesthetic photisms influence her memory for digits. One matrix consisted of black digits, whereas the other two matrices consisted of digits that were either incongruent or congruent with the colors of C's photisms. C's recall of the incongruently colored digits was considerably poorer than her recall of either the black or the congruently colored digits. The 7 nonsynesthetes did not show such differences in their recall of the matrices. In addition, when immediate recall of the black digits was compared with delayed recall of those digits (48 hr), C showed no decrease in performance, whereas each of the nonsynesthetes showed a significant decrease. These findings both demonstrate C's extraordinary memory and show that her synesthetic photisms can influence her memory for digits.     

Changes in attention to relevant and irrelevant stimuli during spatial learning

Rats were trained in 2 experiments to find a submerged platform that was situated in 1 of 2 of the 4 corners of a rectangular pool with a curved long wall. Different landmarks occupied 2 of the corners on every trial, and the platform was always situated near a landmark. For the place group in each experiment, the location of the platform was indicated by the shape of the pool and stimuli outside the pool (place cues), but not the landmarks within the pool. For the landmark groups, the landmarks, not the place cues, indicated where the platform could be found. During Stage 2, 2 of the place cues were relevant, and 2 of the landmarks were irrelevant, for a new discrimination. The place cues better controlled searching for the platform in the place group than in the landmark group when the place cues had initially been relevant by signaling the presence (Experiment 1) or the absence (Experiment 2) of the platform. The results show that animals pay more attention to relevant than irrelevant cues.     

Spatial-frequency-contingent color aftereffects: Adaptation with one-dimensional stimuli

The McCollough effect was shown to be spatial-frequency selective by Lovegrove and Over (1972) after adaptation with vertical colored square-wave gratings separated by 1 octave. Adaptation with slide-presented red and green vertical square-wave gratings separated by 1 octave failed to produce contingent color aftereffects (CAEs).However, when each of these gratings was adapted alone, strong CAEs were produced. Adaptation with vertical colored sine-wave gratings separated by 1 octave also failed to produce CAEs, but strong effects were produced by adaptation with each grating alone. By varying the spatial frequency of the test sine wave, CAEs were found to be tuned for spatial frequency at 2.85 octaves after adaptation of 4 cycles per degree (cpd) and at 2.30 octaves after adaptation of 8 cpd. Adaptation of both vertical and horizontal sine-wave gratings produced strong CAEs, with bandwidths ranging from 1.96 to 2.90 octaves and with lower adapting contrast producing weaker CAEs. These results indicate that the McCollough effect is more broadly tuned for spatial frequency than are simple adaptation effects.     

Analysis of memory modulation by conditioned stimuli

Conditioned stimuli (CS) have multiple psychological functions that can potentially contribute to their effect on memory formation. It is generally believed that CS-induced memory modulation is primarily due to conditioned emotional responses, however, well-learned CSs not only generate the appropriate behavioral and physiological reactions required to best respond to an upcoming unconditioned stimulus (US), but they also serve as signals that the US is about to occur. Therefore, it is possible that CSs can impact memory consolidation even when their ability to elicit conditioned emotional arousal is significantly reduced. To test this, male Sprague–Dawley rats trained on a signaled active avoidance task were divided into “Avoider” and “Non-Avoider” subgroups on the basis of percentage avoidance after 6 d of training. Subgroup differences in responding to the CS complex were maintained during a test carried out in the absence of the US. Moreover, the subgroups displayed significant differences in stress-induced analgesia (hot-plate test) immediately after this test, suggesting significant subgroup differences in conditioned emotionality. Importantly, using the spontaneous object recognition task, it was found that immediate post-sample exposure to the avoidance CS complex had a similar enhancing effect on object memory in the two subgroups. Therefore, to our knowledge, this is the first study to demonstrate that a significant conditioned emotional response is not necessary for the action of a predictive CS on modulation of memory consolidation.

Biologically significant stimuli (unconditioned stimuli [US]) support learning and promote changes in behavior by enhancing the consolidation of memory (White and Milner 1992). Thus, stimuli such as food (Huston et al. 1974, 1977), pain (Galvez et al. 1996; Quirarte et al. 1998), and various drugs of abuse (Krivanek and McGaugh 1969; White 1996; Leri et al. 2013; Rkieh et al. 2014; Wolter et al. 2019, 2020) increase memory storage and facilitate performance on a variety of learning tasks when delivered during a window of memory consolidation that occurs following a learning experience (McGaugh and Roozendaal 2009; Roozendaal and Mcgaugh 2012; McGaugh 2015).Interestingly, exposure to stimuli paired with both incentive (Holahan and White 2013; Wolter et al. 2019, 2020; Baidoo et al. 2020) and aversive (Holahan and White 2002, 2004; Leong et al. 2015; Goode et al. 2016) USs also enhances memory consolidation, presumably because of the conditioned emotional responses that they generate. For example, CSs that precede exposure to footshock elicit freezing (Díaz-Mataix et al. 2017), avoidance (Dombrowski et al. 2013), analgesia (McNally et al. 1999), as well as sympathetic stimulation such as increases in heart rate (Zhang et al. 2019), blood pressure (Hsu et al. 2012), and release of stress hormones (Feenstra et al. 1999), all reactions that are elicited by footshock itself (Lim et al. 1982; McCarty and Baucom 1982; Conti et al. 1990; Galvez et al. 1996; O''Doherty 2004; Lázaro-Muñoz et al. 2010). Holahan and White (2002, 2004) reported that the memory enhancing action of a shock-paired CS could be blocked by lesions of the central amygdala nucleus (CeA), a region involved in generating the behavioral and neurohormonal responses to emotionally arousing stimuli (LeDoux 2003). As well, similarly to a range of aversive USs (anxiogenic drugs, predator odor, tail shock, restraint stress; Kim et al. 2001; Elliott and Packard 2008; Leong and Packard 2014), the effect of a CS paired with footshock on consolidation was found dependent on noradrenergic activation of the amygdala (Goode et al. 2016).However, well-learned CSs not only generate the appropriate behavioral and physiological reactions required to best respond to an upcoming US, but they also serve as signals that the US is about to occur. Temporal relationships between CSs and USs are learned rapidly during conditioning (Ohyama and Mauk 2001; Balsam et al. 2002), and these expectations modulate the expression of learned responses (Holland 2000; Balsam et al. 2010). Moreover, the ability of CSs to predict USs is heavily dependent on mesolimbic dopamine (DA) activity (Schultz et al. 1997; Flagel et al. 2011), and there is substantial evidence that mid-brain DA plays an important role in memory consolidation (White 1989; Managò et al. 2009; Redondo and Morris 2011; Yamasaki and Takeuchi 2017).This analysis suggests that CSs can impact memory consolidation because of their predictive function, even when their ability to elicit preparatory conditioned emotionality is significantly reduced. To test this idea, the current study used a signaled active avoidance task whereby rats learn to avoid an aversive US (footshock) by crossing from one compartment of a shuttle box to another during the presentation of a warning signal. Miller (1948) posited that animals perform the shuttle response during the signal because it prevents the occurrence of the US, and this reduces the experience of conditioned fear caused by the signal. However, it has been found that avoidance persists even when the warning signal no longer elicits a measurable fear state (Kamin et al. 1963; Linden 1969; Coover and Ursin 1973; Starr and Mineka 1977; Mineka and Gino 1980), suggesting that CSs can promote robust avoidance even though conditioned emotional responses are greatly reduced. The current study also used active avoidance because it consistently reveals robust individual differences in learning (Choi et al. 2010; Lázaro-Muñoz et al. 2010; Martinez et al. 2013; Antunes et al. 2020), such that animals can be distinguished into subgroups of Avoiders and Non-avoiders by simple median split (Storace et al. 2019) on percentage avoided USs. Although the source of the individual differences is unknown, it has been postulated the subgroups learn different behavioral responses to the CS (Lázaro-Muñoz et al. 2010; Martinez et al. 2013; Antunes et al. 2020): Avoiders display a loss of fear responses to the CS as the avoidance response is acquired (LeDoux et al. 2017; Cain 2018), while those who fail to acquire the avoidance response continue to display conditioned fear characterized by freezing (Martinez et al. 2013).By capitalizing on these individual differences, the current study explored whether both the predictive and preparatory functions of aversive CSs play a role in modulating consolidation of object memory using the spontaneous object recognition (OR) task. OR relies on the natural tendency of rats to explore novel objects (Winters et al. 2008) and this task was selected because it has been found sensitive to enhancement by exposure to contextual CSs paired with both incentive and aversive stimuli (Wolter et al. 2019, 2020; Baidoo et al. 2020). Given the evidence reviewed above, it was predicted that exposure to the avoidance CS complex (the training chamber, the retractable gate, the warning tone, and the cue light) would impact consolidation of object memory equally in Avoider and Non-Avoider subgroups. Avoider and Non-Avoider subgroups were tested for reactivity to thermal pain throughout avoidance training and testing using the hot-plate to provide an indirect measure of emotional reactivity to the footshock and/or to the aversive CS complex (Fig. 1). This approach was selected because fear/stress-inducing stimuli such as footshock (Maier and Watkins 1991; Rosellini et al. 1994), predator odor (Williams et al. 2005), and their CSs (Hotsenpiller and Williams 1997; McNally and Akil 2001; Ford et al. 2011), elicit stress-induced analgesia; a well-known defensive response in various species (Bolles and Fanselow 1980; Fendt and Fanselow 1999).Open in a separate windowFigure 1.Experimental design used in Experiments 1 and 2.