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How do we measure memory in tricky populations?: Beyond semantic paradigms

By: Anya Singh



Memory is understood as the persistence of learning and retention of information over time, and it is crucial to our daily lives; being able to store, retain, and retrieve memories gives us the ability to reflect on our past, make plans for our future, and more. Researchers have been formally studying memory for over a hundred years, and their insights are fundamental in building our understanding of memory processes and informing how we may treat memory loss.

When you think about memory studies, what procedures come to mind? You may recall the work of Hermann Ebbinghaus, who began the scientific study of memory in 1885 by studying lists of “nonsense syllables” and testing himself on how many he was able to recall (Schwartz, 2017). This method specifically studies semantic memory, or the storage of language-based content in memory, such as words, facts, and meanings. While studies since then have utilized more complex paradigms, many similarly rely on semantic abilities, where the participant must have the capacity to understand a researcher’s instructions and to give a direct indication that they remember an item; for example, a researcher may ask a participant to recite previously learned words or recount a story about the past. After all, if we want to know what someone remembers, why not just ask them directly? 

But there are many forms of memory, and not all populations are suited for semantic paradigms. What if we aren’t able to directly ask an individual what they remember? What if we want to examine the memory of a non-human subject? Researchers have gotten creative in assessing memory for these situations.


Which populations are unfit for semantic memory paradigms?

1. Animals

Researchers studying memory may find animals to be particularly interesting participants, as animals can often serve as simpler models of processes that become more complex in humans. The use of animals as participants also allows researchers to have greater experimental control than they would if their participants were humans; when working with animals, researchers can more easily manipulate variables ranging from living conditions to levels of brain activation, the latter being especially useful when studying the neural components of memory (Capitanio, 2017). 

However, the benefits that come with studying animals are accompanied by some difficulties. Although certain animals have sufficient motor skills and cognitive capacity to carry out experimental tasks, these abilities do not extend to understanding human language. Animals would not be able to understand instructions that researchers give them on how to do a complex task or be able to verbally indicate their memory, such as through reciting previously learned words or recounting a past event. Due to these complications, researchers often cannot use the same common paradigms they use to study memory in human participants to study animals, and instead have to get a bit creative. 

2. Infants

When it comes to humans, the study of memory is not limited to just adults! Researchers are also interested in studying memory in adolescents, children, and infants in particular, focusing on how memory processes differ and evolve throughout humans' early stages of development, as well as how memory plays a crucial role in other aspects of our development. 

Infants constitute another population who are unable to carry out common memory tasks in the same way that human adults are able to. Due to their limited capacity for speech comprehension and production, infants, like animals, would be unable to understand researchers' instructions or provide verbal indicators of their memory. Additionally, infants' lack of motor skills make it hard to carry out alternative physical tasks that researchers may propose. Again, researchers must get creative when studying memory in infants as well!


What paradigms can we use to study memory in these populations?

Animals

When studying animals, learning and memory are typically inferred through observing an animal's behavior that changes as a result of an event or experience. As such, many paradigms used to study memory in animals involve creating an experience that an animal undergoes multiple times—a sort of training—which prompts the animal to then perform a certain action or behave a certain way, with these actions or behaviors serving as indicators of memory. This section will go over two such paradigms that assess spatial and fear memory in animals.

1. Morris Water Maze 

The Morris water maze is a task designed to assess rodents' spatial memory. The water maze itself is a circular pool filled halfway with opaque water; in each trial, a rodent is placed in a new quadrant of the water maze, and the rodent’s goal is to use distal cues—far-away landmarks or markers—to navigate to an escape platform that is hidden in the water (Vorhees & Williams, 2006). Trial after trial, the rodent will become faster at navigating to this platform—the changed behavior of faster navigation as a result of repeated experiences in the water maze is inferred as a demonstration of the rodent's spatial memory. Now, a subsequent “probe trial” can be done to ensure that the rodent is truly using spatial cues, as opposed to proximal or local cues, to navigate to the platform in the water. In this iteration, the platform is taken out of the water, the rodent is placed in a new quadrant of the maze, and researchers observe in which quadrant or quadrants the rodent searches for the platform in. If the rodent spends the majority of its time searching in the target quadrant—the quadrant of the maze that the platform was previously located during training—that is taken as evidence of their spatial memory; if the rodent did not build a spatial memory for the location of the platform, it would spend an equal amount of time in each quadrant.

This paradigm has been used extensively among researchers studying the neurobiology behind learning and memory in particular—researchers can use it to determine the role of different brain regions in memory by comparing rodents' performance on the water maze task before and after a lesion. A classic example comes from Richard G. Morris and his colleagues, who put three groups of rodents through the water maze task—a group with hippocampal damage, a group with neocortical damage, and a group who underwent surgery but sustained no brain damage (Morris et al., 1982). They first found that all three groups performed similarly on a version of the task where the platform was visible above the water, establishing that all groups were capable of navigating towards the platform. During the “probe trial,” they then found that only rodents with hippocampal damage spent equal amounts of time in each quadrant, showing that the hippocampus must remain intact in order to form memory of spatial location. 

2. Fear Conditioning 

Fear conditioning procedures are designed to assess rodents' fear memory. This procedure involves putting a rodent into a novel environment where it can explore, then playing an auditory tone followed by administering a foot shock (Wehner & Radcliffe, 2004; (Curzon, 1970). The foot shock produces freezing—a fear response defined as a "total lack of movement except for respiration"—in the rodent. Over repeated trials, the rodent learns an association between the shock and the tone and conditioning environment, and freezing—a now increased behavior as a result of learning this association—can be quantified as a measure of memory during later tests. Researchers may decide to test for either context or tone memory: memory of the context or spatial cue can be assessed by measuring the rodents’ freezing after placing it in the same environment that it was trained in (contextual fear conditioning), or memory of the auditory cue can be assessed by measuring the rodent’s freezing after playing the tone but while the rodent is placed in a different environment than it was trained in (cued fear conditioning). 

Contextual and cued fear conditioning procedures are also popular in the study of the neurobiology of learning and memory! Researchers can carry out these conditioning procedures, alter something about the rodent's neurobiology, then measure freezing after putting it back in the conditioning context or playing the tone again in order to assess the role of that particular neurobiological component on rodents' fear memory. For example, researchers have assessed the role of certain brain regions on context and tone fear memory by creating lesions to the hippocampus or amygdala in between, and assessed the role of certain receptors in the brain by inactivating NMDA receptors in between. The possibilities are endless! 


Infants

When creating paradigms to study memory in infants, the goal is to take advantage of behaviors that infants produce spontaneously, and to intentionally put infants in contexts where they show these spontaneous behaviors which can serve as indicators of memory. This section will go over three such paradigms that assess episodic memory—the memory of distinct events and experiences—in infants.

1. Visual-Paired Comparison Procedure

The visual-paired comparison procedure takes advantage of the fact that infants like novelty—infants will typically look longer at things they find interesting and rewarding, which are generally things that are novel to them rather than familiar. In this paradigm, infants are shown two identical visual stimuli side by side for a period of time, and after a certain delay, are shown one familiar stimulus and one novel stimulus side by side for a period of time (Fagan, 1990). Memory is then measured by calculating a novelty preference, or the percent of total fixation time that the infant spent looking at the novel stimulus in particular (Fagan, 1990). A higher novelty preference indicates that the infant looked longer at the novel stimulus, which researchers can infer to be a demonstration of their memory for the familiar stimulus; a novelty preference of 0.50 or 50% indicates that an equal amount of time was spent looking at both stimuli, demonstrating a lack of memory for the familiar stimulus. 

Due to the use of an indirect measure for memory, relying on infants' preference for novel items, researchers cannot go further to establish the content of these infants' memories using this paradigm. However, a great advantage of this procedure is that it is highly adaptable—it is easy to modify aspects of this paradigm to answer various questions about infants' memory. For example, researchers can use this paradigm to assess the nature of encoding, by altering the amount of time that infants are exposed to the initial stimuli; storage, by altering the duration of the delay; and retrieval, by altering the context or environment that infants retrieve the stimulus in.

2. Mobile Conjugate Reinforcement Paradigm

The mobile conjugate reinforcement paradigm takes advantage of the fact that infants will repeat an action if it results in a desirable outcome—in this case, repeating a kicking action to result in movement from a mobile. In this paradigm, infants lay in a crib with an overhead mobile and have a silk cord tied loosely around their ankle (C. K. Rovee & D. T. Rovee, 1969). Researchers measure the number of times an infant kicks during a baseline period, or while their leg is connected to a stationary part of its crib, in order to get a sense of how much an infant kicks on its own; during an acquisition period, or while their leg is connected to the mobile which moves as a result of the infants' kicking movement, to allow the infant to establish an association between the two events; and again during both immediate and long-term retention tests, or while the infant's leg is no longer attached to the mobile, allowing researchers to observe if the infant displays more kicking behavior than in the baseline phase as a result of the conditioning procedure (C. K. Rovee & D. T. Rovee, 1969). Here, memory can be measured by calculating a retention ratio by dividing the kicking rate during the long-term retention test by the kicking rate during the immediate retention test; a higher retention ratio indicates stronger memory.

Similar to the visual-paired comparison procedure, while researchers can infer the infants' memory through the use of this indirect measure,, they aren't able to determine the actual content of the memory. However, the mobile conjugate reinforcement paradigm is also easy to adapt for a variety of research questions. Researchers can assess the effects of amount of exposure on encoding by altering the duration of the baseline period, the effects of context change on retrieval by altering the appearance of the crib, and the effects of retention intervals by altering the amount of delay between the immediate and long-term retrieval tests.

3. Imitation Procedure

The imitation procedure takes advantage of infants' behavioral tendency to imitate actions. In this paradigm, infants are given a set of physical objects and researchers observe whether or not infants perform a specific sequence of actions with those objects, perform their own play, etc. during a pre-modeling baseline period (​​Lukowski & Milojevich, 2016). Next, a researcher models a sequence of actions with an accompanying narration and the infant is given a chance to imitate the actions either immediately or after a delay. Memory is measured in these retention tests through the number of actions an infant remembers to imitate compared to the number of actions performed in the baseline period, with a higher amount of imitated actions indicating stronger or better memory.

A disadvantage of this paradigm is that it puts an additional emphasis on the temporal relations within memories and requires infants to have a certain extent of motor control to be able to imitate these actions. However, unlike the previous two paradigms, researchers using the imitation procedure can directly measure memory as the number of actions an infant remembers and are able to gain more insight on the content of a memory. Additionally, this paradigm can be altered to further study the effect of the number of actions, type of actions, amount of exposure, and context changes (regarding both changes in objects and environment) on infants' memory.


Conclusion

Researchers have come up with a variety of creative paradigms to use in the experimental study of memory specifically in populations of participants where obtaining measures of their memory may not be so straightforward. While differences in these populations generally call for different general approaches, many of the paradigms outlined in this article are drawn up from similar concepts and are highly adaptable; using this starting point to understand the strengths and limitations across these paradigms can be useful in considering how they may be applicable in your own research endeavors and towards expanding your research toolkit! 


References

Capitanio, J. (2017, January). Animal studies in psychology. American Psychological Association. https://www.apa.org/ed/precollege/psn/2017/01/animal-studies.


Curzon, P., Rustay, N. R., & Browman, K. E. (1970, January 1). Cued and Contextual Fear Conditioning for Rodents. Methods of Behavior Analysis in Neuroscience. 2nd edition. https://www.ncbi.nlm.nih.gov/books/NBK5223/#:~:text=If%2C%20in%20a%20given%20environment,shock%20in%20the%20near%20future 


Fagan, J. F. (1990). The Paired-Comparison Paradigm and Infant Intelligence. Annals of the New York Academy of Sciences, 608(1), 337–364. https://doi.org/10.1111/j.1749-6632.1990.tb48902.x   


​​Lukowski, A. F., & Milojevich, H. M. (2016). Examining Recall Memory in Infancy and Early Childhood Using the Elicited Imitation Paradigm. Journal of Visualized Experiments, (110). https://doi.org/10.3791/53347 


Morris, R. G., Garrud, P., Rawlins, J. N., & O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681–683. https://doi.org/10.1038/297681a0 


Rovee, C. K., & Rovee, D. T. (1969). Conjugate reinforcement of infant exploratory behavior. Journal of Experimental Child Psychology, 8(1), 33–39. https://doi.org/10.1016/0022-0965(69)90025-3


Schwartz, B. L. (2017). Introduction to the Study of Memory. In Memory: Foundations and Applications (4th ed., pp. 1–33). essay, SAGE Publications, Inc. 


Vorhees, C. V., & Williams, M. T. (2006). Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nature Protocols, 1(2), 848–858. https://doi.org/10.1038/nprot.2006.116 


Wehner, J. M., & Radcliffe, R. A. (2004). Cued and contextual fear conditioning in mice. Current Protocols in Neuroscience, 27(1). https://doi.org/10.1002/0471142301.ns0805cs27 

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