Survival often depends on animals’ ability to make split-second decisions that rely on imagining alternative futures: If I’m being chased by a hungry predator, do I zag left to get home safely or zig right to lead the predator away from my family?
When two paths diverge in a yellow wood, which will lead me to breakfast and which will lead me to become breakfast?
Both look really about the same, but imagination makes all the difference.
In a study of rats navigating a simple maze, neuroscientists at UC San Francisco have discovered how the brain may generate such imagined future scenarios.
The work provides a new grounding for understanding not only how the brain makes decisions but also how imagination works more broadly, the researchers say.
“One of the brain’s most amazing abilities is to imagine things that aren’t right in front of it,” said Loren Frank, PhD, a professor of physiology and Howard Hughes Medical Institute investigator in the UCSF Center for Integrative Neuroscience, co-director of the UCSF Kavli Institute for Fundamental Neuroscience, and member of the UCSF Weill Institute for Neurosciences.
“Imagination is fundamental to decision-making, but so far neuroscience hasn’t given a good explanation of how the brain generates imagined futures in real time to inform various kinds of everyday decisions — while keeping track of reality at the same time.”
In the new study, published January 30, 2020, in Cell, Frank’s team had rats explore an M-shaped maze, while recording the firing of neurons in the hippocampus called “place cells”, which are traditionally thought to keep track of an animal’s location — like a neural GPS system.
But as the rats approached a fork in the maze, the researchers discovered that their place-cell activity began to switch back and forth extremely rapidly — at a rate of eight times per second — between representing the animal’s current position and its two alternative future paths, as if to say: “Here I am — go left? — here I am — go right?”
The team also extended this finding to another type of imagined scenario. Apart from location, place cells have also been known to keep track of an animal’s travel direction.
The team found that place cells representing opposite travel directions could also switch back and forth extremely rapidly, as if to say, “I’m going this way, but I could also turn around and go the other way.”
“The cells’ fast switching between present and possible paths was unmistakable because it was so regular,” said Kenneth Kay, PhD, a post-doctoral researcher at Columbia University who led the study as a graduate student in Frank’s lab.
“It was exciting to see because speed plus consistency is exactly what’s needed in any number of real-world settings, for both animals and humans.”
The place cells’ oscillations between the present and possible futures didn’t appear to be directly controlling rats’ decisions about which path to choose, but did become stronger as the rats approached the decision point, Kay and colleagues found.
This suggested to the researchers that the role of the hippocampus in decision-making might be to generate a “menu” of imagined scenarios for other parts of the brain that can associate these options with past experience of their value or potential danger, then make an appropriate decision based on the animal’s current drives — hungry or thirsty, fearful or bold.
“We think this shows that the hippocampus is not just responsible for the recording the past and processing the present, but for imagining the future as well,” Frank said.
“This study is just a first step, but it opens new avenues for us to study how imagined scenarios are generated and evaluated in the brain as animals make decisions.”
Study Suggests New Conception of Hippocampus as Source of Imagination
The hippocampus, a seahorse-shaped structure found on each side of the brain deep in the temporal lobes, is among the most intensively studied parts of the brain.
“We think this shows that the hippocampus is not just responsible for the recording the past and processing the present, but for imagining the future as well,” Frank said.
Hippocampal damage — whether by brain injury or in a disease such as Alzheimer’s — robs people of the ability to form new memories, leading 20th century scientists to describe the hippocampus as the brain’s memory center.
In the 1970s, scientists identified hippocampal place cells, which spontaneously create maps of new environments as animals explore them, then store these maps for later use. This discovery, which was awarded the 2014 Nobel Prize in Physiology or Medicine, prompted scientists to recognize that the hippocampus is also a navigation center — responsible for, say, allowing an animal to find its way back to the place where it remembers eating those delicious blackberries last summer.
Along these lines, previous work by Frank and others has shown that place cell activity can replay an animal’s recent movements or even anticipate where an animal may be headed next, but such activity had only been seen intermittently — typically when animals were resting or pausing during ongoing movement — as actively considering their next move.
The new Cell study is the first to show how hippocampal cells can represent different hypothetical scenarios consistently and systematically over time. Such a system could allow animals on the move to make extremely rapid decisions in the moment based on these imagined alternatives while also keeping track of the animal’s present reality, the researchers say. It could even play a role in the brain’s ability to generate hypothetical scenarios or thoughts more broadly.
“The regular switching between present and possible — or actual and imagined — looks like be a robust system for generating lots of ideas, not just for mechanically remembering or predicting,” Kay said. “The hippocampus could be at the root of our ability to imagine.”
Authors: Additional authors on the study were Jason Chung, Marielena Sosa, Jonathan S. Schor, Mattias Karlsson, Margaret Larkin, and Daniel Liu of UCSF.
Funding: The research was supported by the Howard Hughes Medical Institute, the Simons Collaboration for the Global Brain (521921, 542981), the National Institutes of Health (R01 MH090188, R01 MH105174), the National Science Foundation (NSF) NeuroNex Award (DBI-1707398), and the Gatsby Charitable Foundation.
The authors declare no competing interests.
Our daily lives consist of a continuous stream of information. Yet like chapters in a book, we usually remember past experiences as distinct and meaningful events. For instance, a typical morning might be remembered as a series of discrete activities linked to a specific place and time, such as eating breakfast at home and then driving to work.
The features of these autobiographical episodes are also not represented equally in memory: someone might recall a torturous commute to work as taking much longer than simply eating breakfast in their living room, even if the actual duration of these events was the same. These scenarios emphasize the fact that our memories are not veridical records of the past.
Rather, they reflect discrete “units” of subjective experience. But what is it about these situations that lead to differences in how they are represented in memory? How do our thoughts, feelings, and surroundings integrate the elements of ongoing experience into temporally organized events?
Influential models of event perception posit that individuals perceive shifts in spatial or perceptual context, such as stepping through a doorway, as “event boundaries” (Radvansky, 2012; Zacks et al., 2007). It is thought that the ability to segment continuous sensory inputs is highly adaptive, because it unburdens the mind of fleeting and potentially obsolete working memory representations.
By helping reorient attention to salient environmental changes, such as a sudden switch in one’s actions, intentions, or surroundings (Bailey et al., 2017; Khemlani et al., 2015; Zwaan & Radvansky, 1998), these boundaries are theorized to trigger brain mechanisms that update ongoing mental representations of the current state, or context (Richmond & Zacks, 2017; Zacks & Sargent, 2010).
The updating of these active ‘event models’ may in turn promote the selection of behaviors best suited to the current environment. Prior research has largely focused on cognitive and neural processes that enable us to perceive discrete events. More recently, progress has been made in identifying how boundaries impact the long-term organization of episodic memory (Clewett & Davachi, 2017).
At the behavioral level, many types of context shifts, including narrative (Zwaan et al., 1995; Zwaan & Radvansky, 1998), spatial, (Radvansky & Copeland, 2006), motion (Zacks, 2004), and other perceptual shifts (Sridharan et al., 2007; Swallow et al., 2011; Swallow et al., 2009) have been demonstrated to not only influence how we perceive discrete events but also to influence how we remember the temporal aspects of those prior episodes (Davachi & DuBrow, 2015; DuBrow & Davachi, 2013, 2014, 2016; Ezzyat & Davachi, 2011, 2014; Heusser et al., 2018; Horner et al., 2016; Lositsky et al., 2016; Sols et al., 2017; Figure 1).
For instance, when studying a list of information, items that appear sequentially are more likely to be “bound” together, facilitating memory for the order in which they occurred. However, if items appear on either side of an event boundary (e.g., moving from one room to another), their sequential binding is reduced.
That is, individuals are more likely to forget the precise order of item pairs if they spanned an intervening context shift (DuBrow & Davachi, 2013, 2014, 2016; Ezzyat & Davachi, 2011; Heusser et al., 2018; Horner et al., 2016; Sols et al., 2017).
Event boundaries can also modulate how we remember time itself, particularly by dilating subjective time duration. Items spanning boundaries tend to be remembered as happening farther apart in time, despite having the same true temporal distance (Ezzyat & Davachi, 2014; Lositsky et al., 2016).
In a similar vein, the number and complexity of context changes (e.g., how elaborate ongoing changes in stimulus features are) have been shown to increase duration estimates for the entire length of recent events (Faber & Gennari, 2015, 2017; Waldum & Sahakyan, 2013).
Together these findings have emphasized the importance of contextual overlap in determining whether incoming information becomes integrated into a unified memory representation.
At the neural level, decades of lesion, physiology and imaging methods have implicated the hippocampus, medial temporal cortical regions (MTL), and the prefrontal cortex in distinct aspects of memory formation (Eichenbaum, 2004, 2017; Howard & Eichenbaum, 2013; Morton et al., 2017; Polyn & Kahana, 2008; Tulving, 1972, 2002).
In particular, these regions have been implicated in different aspects of relational memory binding by which individual items are encoded with specific details about when they occurred, where they occurred, and their perceptual features.
More broadly, research also implicates these neural mechanisms in being essential for memory integration, the concept that experiences with overlapping contextual or featural information also become stored as overlapping neural representations (Schlichting & Preston, 2015). This overlap in turn enables similar information, including both existing memories and novel information, to become linked together in memory.
There has been a surge of work in recent years highlighting the individual and coordinated roles of these structures in binding sequential representations of discrete mnemonic events (DuBrow & Davachi, 2016; Ezzyat & Davachi, 2011, 2014; Fortin et al., 2002; Howard & Eichenbaum, 2013; Hsieh et al., 2014; Hsieh & Ranganath, 2015; Jenkins & Ranganath, 2010; Kalm et al., 2013; Kesner et al., 2002; Schapiro et al., 2012; Schapiro et al., 2013).
What has emerged from this body of work is a remarkable synergy between findings in humans and animals, thereby underscoring the evolutionarily conserved roles of these structures in episodic memory organization (Eichenbaum, 2017; Panoz-Brown et al., 2016; Panoz-Brown et al., 2018; Preston & Eichenbaum, 2013).
This research has also drawn intriguing parallels between the brain mechanisms that link events together either during learning or after longer delays (Schlichting & Frankland, 2017), raising the possibility that similar or complementary mechanisms are involved in the formation and integration of episodic memories at different timescales (e.g., Mau et al., 2018; Nielson et al., 2015; Wirt & Hyman, 2017).
In humans, functional magnetic resonance imaging (fMRI) has provided an invaluable tool for investigating how boundaries shape memory representations in the brain. By inserting even the simplest change in sequence learning tasks, such as changing the location of an item or changing the visual category of a stimulus, researchers have begun to characterize encoding patterns of brain activity that can predict the temporal organization of events in long-term memory (for reviews see Brunec et al., 2018; Clewett & Davachi, 2017). Much of this work has focused on identifying neural measures of event organization to understand how the brain forms memories for distinct episodes.
These methods include examining how event structure modulates average BOLD activation signal both in individual brain regions as well as in the functional coupling between regions that contribute to attention and memory processing (e.g., DuBrow & Davachi, 2016; Ezzyat & Davachi, 2014).
The advent of multivoxel pattern analyses, which target similarities and differences in neural representations across different stimuli or time points, has also provided an effective measure of neural encoding and retrieval signatures that may be obscured by more spatially coarse-grained univariate BOLD signal analyses (DuBrow & Davachi, 2014; Ezzyat & Davachi, 2014; Lositsky et al., 2016; Ritchey et al., 2012). Through these diverse techniques, neuroimaging studies have shed new light on the kinds of brain activity that respond to event boundaries and that define ‘events’ themselves.
These neural measures also reveal the neural processes that may influence the temporal aspects of remembering, including memory for temporal order, temporal duration, and temporal distance between items from recent sequences (Davachi & DuBrow, 2015; Ranganath & Hsieh, 2016).
In this review, we synthesize evidence that temporal stability and change in context representations influence the neural and computational processes that integrate and separate episodic memories across time.
We begin with findings suggesting that, at relatively short timescales of learning, hippocampal and cortical memory integration processes track regularities in experience, such as similarities in perceptual features over time, to support the encoding of order and temporal distance between sequential items. This formation of meaningful episodes can occur both proactively,or as a new or familiar event unfolds, as well as retroactively, or after a context shift has occurred.
We primarily focus on evidence from human fMRI studies and, when relevant, rodent studies that inform the causal relationships how different brain regions communicate during sequence learning. We also foreground evidence that goal states may play a key role in regulating the influence of context shifts on temporal memory processes.
Next, we discuss work examining memory integration and separation processes and their behavioral correlates at relatively longer timescales. This includes new research showing that temporal proximity helps determine whether gradually evolving patterns of hippocampal and PFC activity integrates or separate memories for events that share overlapping information.
We also review fMRI findings suggesting that hippocampal retrieval processes may serve to transcend larger gaps in time to bind context-appropriate information in memory.
We conclude with research showing that boundaries also modulate non-temporal aspects of episodic memory, including memory for individual items and their surrounding source information (Figure 1). Through this review, we aim to provide a holistic view of the factors and neural processes that shape the long-term organization of episodic memory.
Source:
UCSF
