Premembering Experience: A Hierarchy of Time-Scales for Proactive Attention
Authors: Anna C. Nobre, Mark G. Stokes
Journal: Neuron (2019)

Memories are about the past, but they serve the future. Memory research often emphasizes the former aspect: focusing on the functions that re-constitute (re-member) experience and elucidating the various types of memories and their interrelations, timescales, and neural bases. Here we highlight the prospective nature of memory in guiding selective attention, focusing on functions that use previous experience to anticipate the relevant events about to unfold—to "premember" experience. Memories of various types and timescales play a fundamental role in guiding perception and performance adaptively, proactively, and dynamically. Consonant with this perspective, memories are often recorded according to expected future demands. Using working memory as an example, we consider how mnemonic content is selected and represented for future use. This perspective moves away from the traditional representational account of memory toward a functional account in which forward-looking memory traces are informationally and computationally tuned for interacting with incoming sensory signals to guide adaptive behavior. Memories are about the past, but they serve the future. Memory research often emphasizes the former aspect: focusing on the functions that re-constitute (re-member) experience and elucidating the various types of memories and their interrelations, timescales, and neural bases. Here we highlight the prospective nature of memory in guiding selective attention, focusing on functions that use previous experience to anticipate the relevant events about to unfold—to "premember" experience. Memories of various types and timescales play a fundamental role in guiding perception and performance adaptively, proactively, and dynamically. Consonant with this perspective, memories are often recorded according to expected future demands. Using working memory as an example, we consider how mnemonic content is selected and represented for future use. This perspective moves away from the traditional representational account of memory toward a functional account in which forward-looking memory traces are informationally and computationally tuned for interacting with incoming sensory signals to guide adaptive behavior. Memory's most compelling illusion is that it represents the past. However, it is clear from an ecological perspective that memory is all about the future. The purpose of memory is to learn about the environment to anticipate future demands—not just putting back the pieces of the past for recollection (remembering experience) but deriving possibilities based on the past to guide future adaptive behavior (premembering experience). This notion has old roots (Helmholtz, 1867Helmholtz H. Handbuch der Physiologischen Optik.in: Karsten G. Allgemeine Encyklopadie der Physik, Volume 9. Leipzig: Voss, 1867: 37-51Google Scholar), but, surprisingly, the fundamental operations through which memories guide adaptive behavior lack an established theoretical framework, and their mechanisms have yet to capture the in-depth and systematic investigation they deserve. We propose that memory, over a broad hierarchy of timescales, supplies the essential elements for selective attention to guide perception and performance flexibly and adaptively. We introduce the term "premembering" to capture this prospective and dynamic role of memory. Our construct complements proposals for how memories can be used to inform other cognitive functions, such as adaptive control, decision-making, and imagining future situations (Box 1).BOX 1Prospective Memories in Different Cognitive DomainsWe focus on how memories guide selective attention. The role memory plays in guiding behavior has also been considered within other cognitive domains."Cognitive control" refers to the collection of mechanisms that set and adjust our goals and that monitor and regulate performance according to competing demands. Thus, the selective attention mechanisms we review are subordinate to cognitive control, prioritizing and selecting putative targets and overcoming irrelevant distraction within a particular goal setting. Memories are increasingly recognized to play an important role in influencing the degree of top-down control exerted on a given trial. They include both short-term traces between successive trials as well as intermediate memory traces that develop over task performance (Chiu and Egner, 2019Chiu Y.C. Egner T. Cortical and subcortical contributions to context-control learning.Neurosci. Biobehav. Rev. 2019; 99: 33-41Crossref PubMed Scopus (6) Google Scholar)."Decision-making" refers to the process of choosing one of a set of alternatives to produce a beneficial outcome. Choices are made based on expectation of rewards developed through previous experience. Current models of decision-making mostly rely on reinforcement learning. Recent computational studies suggest that different types of memory traces may work together to optimize reinforcement learning, including those resulting from slow incremental implicit learning over trials as well as episodic traces uniquely linked to individual experiences (Botvinick et al., 2019Botvinick M. Ritter S. Wang J.X. Kurth-Nelson Z. Blundell C. Hassabis D. Reinforcement learning, fast and slow.Trends Cogn. Sci. 2019; 23: 408-422Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar)."Decision-making" is closely related to selective attention, which can be involved in prioritizing information for guiding choice behavior. Expectations play an essential role in both sets of processes. However, interestingly, they each stress a different consequence of prior knowledge. In decision-making, predictions based on priors are mainly used to attenuate the processing of what can be anticipated (Friston, 2010Friston K. The free-energy principle: a unified brain theory?.Nat. Rev. Neurosci. 2010; 11: 127-138Crossref PubMed Scopus (1759) Google Scholar). In selective attention, predictions are mainly used to enhance the processing of anticipated task-relevant information. These two phenomena nicely illustrate the flexibility with which memory-related traces can be used to guide adaptive performance. The specific consequence of prior knowledge will be heavily dependent on the purpose of the task (Nobre, 2018Nobre A.C. Attention.in: Wixted J.T. Thompson-Schill S.L. Stevens' Handbook of Experimental Psychology and Cognitive Neuroscience, Volume 2, Sensation, Perception and Attention. Fourth Edition. John Wiley & Sons, 2018: 241-316Crossref Google Scholar)."Episodic future thinking" involves drawing on previous experiences to imagine oneself in future situations (Atance and O'Neill, 2001Atance C.M. O'Neill D.K. Episodic future thinking.Trends Cogn. Sci. 2001; 5: 533-539Abstract Full Text Full Text PDF PubMed Scopus (532) Google Scholar, Schacter et al., 2008Schacter D.L. Addis D.R. Buckner R.L. Episodic simulation of future events: concepts, data, and applications.Ann. N Y Acad. Sci. 2008; 1124: 39-60Crossref PubMed Scopus (459) Google Scholar). The construct is useful in different types of situations, such as navigation, planning to implement intentions, understanding others' mental states, and simulating future events. Neuropsychological, developmental, and brain imaging studies have revealed substantial overlap between the neural system supporting episodic future thinking and episodic recollection, suggesting that the LTM traces available for recollection can also be used prospectively and flexibly to build novel plausible scenarios and run simulations (Schacter et al., 2008Schacter D.L. Addis D.R. Buckner R.L. Episodic simulation of future events: concepts, data, and applications.Ann. N Y Acad. Sci. 2008; 1124: 39-60Crossref PubMed Scopus (459) Google Scholar). Episodic future thinking differs from our construct of premembering in being a specifically deliberative process based on LTM traces available to awareness to inform behavior in the future. Premembering is a broader construct, considering the influences of memories of different types and timescales on ongoing or imminent behavior. We focus on how memories guide selective attention. The role memory plays in guiding behavior has also been considered within other cognitive domains."Cognitive control" refers to the collection of mechanisms that set and adjust our goals and that monitor and regulate performance according to competing demands. Thus, the selective attention mechanisms we review are subordinate to cognitive control, prioritizing and selecting putative targets and overcoming irrelevant distraction within a particular goal setting. Memories are increasingly recognized to play an important role in influencing the degree of top-down control exerted on a given trial. They include both short-term traces between successive trials as well as intermediate memory traces that develop over task performance (Chiu and Egner, 2019Chiu Y.C. Egner T. Cortical and subcortical contributions to context-control learning.Neurosci. Biobehav. Rev. 2019; 99: 33-41Crossref PubMed Scopus (6) Google Scholar)."Decision-making" refers to the process of choosing one of a set of alternatives to produce a beneficial outcome. Choices are made based on expectation of rewards developed through previous experience. Current models of decision-making mostly rely on reinforcement learning. Recent computational studies suggest that different types of memory traces may work together to optimize reinforcement learning, including those resulting from slow incremental implicit learning over trials as well as episodic traces uniquely linked to individual experiences (Botvinick et al., 2019Botvinick M. Ritter S. Wang J.X. Kurth-Nelson Z. Blundell C. Hassabis D. Reinforcement learning, fast and slow.Trends Cogn. Sci. 2019; 23: 408-422Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar)."Decision-making" is closely related to selective attention, which can be involved in prioritizing information for guiding choice behavior. Expectations play an essential role in both sets of processes. However, interestingly, they each stress a different consequence of prior knowledge. In decision-making, predictions based on priors are mainly used to attenuate the processing of what can be anticipated (Friston, 2010Friston K. The free-energy principle: a unified brain theory?.Nat. Rev. Neurosci. 2010; 11: 127-138Crossref PubMed Scopus (1759) Google Scholar). In selective attention, predictions are mainly used to enhance the processing of anticipated task-relevant information. These two phenomena nicely illustrate the flexibility with which memory-related traces can be used to guide adaptive performance. The specific consequence of prior knowledge will be heavily dependent on the purpose of the task (Nobre, 2018Nobre A.C. Attention.in: Wixted J.T. Thompson-Schill S.L. Stevens' Handbook of Experimental Psychology and Cognitive Neuroscience, Volume 2, Sensation, Perception and Attention. Fourth Edition. John Wiley & Sons, 2018: 241-316Crossref Google Scholar)."Episodic future thinking" involves drawing on previous experiences to imagine oneself in future situations (Atance and O'Neill, 2001Atance C.M. O'Neill D.K. Episodic future thinking.Trends Cogn. Sci. 2001; 5: 533-539Abstract Full Text Full Text PDF PubMed Scopus (532) Google Scholar, Schacter et al., 2008Schacter D.L. Addis D.R. Buckner R.L. Episodic simulation of future events: concepts, data, and applications.Ann. N Y Acad. Sci. 2008; 1124: 39-60Crossref PubMed Scopus (459) Google Scholar). The construct is useful in different types of situations, such as navigation, planning to implement intentions, understanding others' mental states, and simulating future events. Neuropsychological, developmental, and brain imaging studies have revealed substantial overlap between the neural system supporting episodic future thinking and episodic recollection, suggesting that the LTM traces available for recollection can also be used prospectively and flexibly to build novel plausible scenarios and run simulations (Schacter et al., 2008Schacter D.L. Addis D.R. Buckner R.L. Episodic simulation of future events: concepts, data, and applications.Ann. N Y Acad. Sci. 2008; 1124: 39-60Crossref PubMed Scopus (459) Google Scholar). Episodic future thinking differs from our construct of premembering in being a specifically deliberative process based on LTM traces available to awareness to inform behavior in the future. Premembering is a broader construct, considering the influences of memories of different types and timescales on ongoing or imminent behavior. Selective attention (hereafter called "attention") refers to the set of functions that prioritize and select information to guide adaptive behavior (Nobre, 2018Nobre A.C. Attention.in: Wixted J.T. Thompson-Schill S.L. Stevens' Handbook of Experimental Psychology and Cognitive Neuroscience, Volume 2, Sensation, Perception and Attention. Fourth Edition. John Wiley & Sons, 2018: 241-316Crossref Google Scholar). These functions modulate incoming sensory signals and influence their processing at multiple stages to inform awareness, decisions, actions, and subsequent memories. It has long been appreciated that short-term memory, or "working memory" (WM), plays an important role in forming attentional templates (e.g., Desimone and Duncan, 1995Desimone R. Duncan J. Neural mechanisms of selective visual attention.Annu. Rev. Neurosci. 1995; 18: 193-222Crossref PubMed Google Scholar). Here we suggest that WM is part of a much larger family of heterogenous attention-guiding memory traces that span multiple timescales. The premembering perspective has important implications for understanding the content and formatting of memory. Rather than slavishly storing and using veridical traces, the brain flexibly selects and even distorts memory content to enhance its utility in guiding attention. Moreover, task-relevant informational content may also be stored in a neural format that is optimized for the anticipated utilization of the memory to guide performance. The essence of memory is the traces left by passing experience. These range from transient perturbations to engrams that last a lifetime, capturing modality-specific fragments to relational and integrated wholes and supporting unconscious states to recollective phenomena. Such traces can provide essential informational content required for prospectively prioritizing and selecting what is important. Working together, memory content and attention functions shape how the brain transforms incoming signals to guide perception, choice, action, and the formation of new memories to serve adaptive behavior in the future (Figure 1). It can be argued that these prospective properties of memory are what define its fundamental ecological purpose: to collect relevant aspects of experience to anticipate future demands and guide behavior. Drawing a clear line defining when present becomes past may be impossible. Nevertheless, it is clear that past traces affect perception even from their earliest moments. The very stitching of visual perception across eye movements into an apparent cohesive flow may rely on short-term memories bridging the anchoring and landing fixation contents (Irwin and Gordon, 1998Irwin D.E. Gordon R.D. Eye movements, attention and trans-saccadic memory.Visual Cognition. 1998; 5: 127-155Crossref Google Scholar). Furthermore, transient salient visual stimuli intrinsically capture attention and leave a brief excitatory trail, temporarily enhancing processing of stimuli that follow in their immediate wake (Posner, 1980Posner M.I. Orienting of attention.Q. J. Exp. Psychol. 1980; 32: 3-25Crossref PubMed Google Scholar; Figure 2A). At slightly longer timeframes, WM provides a limited set of more durable traces that are independent of continuous sensory stimulation and resistant to interference and that act to guide adaptive behavior (Baddeley, 2003Baddeley A. Working memory: looking back and looking forward.Nat. Rev. Neurosci. 2003; 4: 829-839Crossref PubMed Scopus (2500) Google Scholar). The fundamental role WM plays in guiding attention is widely recognized and has been studied extensively (Desimone and Duncan, 1995Desimone R. Duncan J. Neural mechanisms of selective visual attention.Annu. Rev. Neurosci. 1995; 18: 193-222Crossref PubMed Google Scholar). 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