A roadmap for understanding memory: Decomposing cognitive processes into operations and representations Rosemary A. Cowella*, Morgan D. Barenseb, Patrick S. Sadila a. Department of Psychological and Brain Sciences, University of Massachusetts Amherst, MA 01003, USA b. Department of Psychology, University of Toronto, Toronto, Ontario M5S 3G3, Canada • Author Contributions: R.A.C. wrote the initial draft of the paper; R.A.C., M.D.B. and P.S.S. contributed to review and editing of subsequent drafts. • Corresponding Author: Rosemary A. Cowell, Department of Psychological and Brain Sciences, University of Massachusetts Amherst, MA 01003, USA. Email: [email protected]. • Number of Figures: 3 • Number of Tables: 0 • Number of Words, Abstract: 246 • Number of Words, Significance Statement: 120 • Number of Words, Main Text (Introduction through Conclusion, including Box): 7,131 • Acknowledgements: R.A.C. was funded by NSF award 1554871 and NIMH award 1RF1MH114277. M.D.B. was funded by the Canada Research Chairs Program, a Scholar Award from the James S McDonnell Foundation, a Discovery Grant and Accelerator Supplement from the National Science and Engineering Council of Canada, and a Project Grant from the Canadian Institutes of Health Research. The authors would like to thank Chuck Clifton and Tim Bussey for helpful discussions. • Conflicts of Interest: Authors report no conflict of interest. • Funding Sources: R.A.C. was funded by NSF award 1554871 and NIMH award 1RF1MH114277. M.D.B. was funded by the Canada Research Chairs Program, a Scholar Award from the James S McDonnell Foundation, a Discovery Grant and Accelerator Supplement from the National Science and Engineering Council of Canada, and a Project Grant from the Canadian Institutes of Health Research. 1 Abstract Thanks to patients Phineas Gage and Henry Molaison, we have long known that behavioral control depends on the frontal lobes, whereas declarative memory depends on the medial temporal lobes. For decades, cognitive functions – behavioral control, declarative memory – have served as labels for characterizing the division of labor in cortex. This approach has made enormous contributions to understanding how the brain enables the mind, providing a systems-level explanation of brain function that constrains lower-level investigations of neural mechanism. Today, the approach has evolved such that functional labels are often applied to brain networks rather than focal brain regions. Furthermore, the labels have diversified to include both broadly-defined cognitive functions (declarative memory, visual perception) and more circumscribed mental processes (recollection, familiarity, priming). We ask whether a process – a high-level mental phenomenon corresponding to an introspectively-identifiable cognitive event – is the most productive label for dissecting memory. For example, the process of recollection conflates a neurocomputational operation (pattern completion-based retrieval) with a class of representational content (associative, high-dimensional, episodic-like memories). Because a full theory of memory must identify operations and representations separately, and specify how they interact, we argue that processes like recollection constitute inadequate labels for characterizing neural mechanisms. Instead, we advocate considering the component operations and representations of mnemonic processes in isolation, when examining their neural underpinnings. For the neuroanatomical organization of memory, the evidence suggests that pattern completion is recapitulated widely across cortex, but the division of labor between cortical sites can be explained by representational content. Significance Statement Accounts of cognition often assume that the brain is organized along lines of cognitive process, for example, with recollection mediated by one neural structure and familiarity by another. We argue that cognitive processes – introspectively-identifiable mental events like recollection – are inadequate labels for characterizing neural mechanisms, because they conflate lower-level components of the mechanisms we seek to identify. Recollection involves both a neurocomputational operation (pattern completion) and a neural representation (high-dimensional, associative content). To uncover memory's mechanisms, we must decompose cognitive processes into their operations and representations, asking how each contributes to the production of neural and behavioral phenomena. For the neuroanatomical organization of memory, decomposing recollection reveals that the factor with the greatest explanatory power is representational content. 2 Introduction Since Phineas Gage and Patient H.M., we have known that distinct cognitive abilities can be mapped onto discrete brain regions: key aspects of behavioral control depend on the frontal lobes, whereas the ability to form long-term declarative memories depends on the medial temporal lobes. The topological framework provided by such mappings offers valuable systems-level explanations of brain function that critically constrain lower-level investigations of neural mechanism. Thus, a major goal of cognitive neuroscience could be crudely characterized as a well-founded game of pin the tail on the donkey, in which “blindfolded” researchers pin cognitive functions to the cerebral cortex. This approach has made enormous contributions to understanding how the brain enables the mind. Today, the approach has evolved such that the functional labels are often applied to brain networks rather than focal brain regions. Furthermore, the labels describing the division of labor have diversified to include both broadly- defined cognitive functions (declarative memory versus visual perception, short-term versus long-term memory) and more circumscribed mental processes (recollection versus familiarity). In this review we take recollection as an example, asking whether this process-based account provides the best description of the available data concerning how different brain regions contribute to declarative memory. If not, what alternative set of labels could be applied to cortical sites to capture the neuroanatomical organization of memory? What is recollection? Recollection has a long history as an explanatory construct in experimental and cognitive psychology. A recollection-like process was described in detail by William James in 1890, and has since been invoked by many authors in various guises – an intentional search of memory; the effortful retrieval of context and detail; autonoetically-conscious remembering (Hasher and Zacks, 1979; Tulving, 1985; Jacoby, 1991). In modern memory theories, recollection is typically defined as a pattern-completion-like retrieval mechanism, in which a cue (external or internal) prompts the conscious remembering of specific details of an episode (Marr, 1971; Tulving, 1982; Rolls, 1996; Norman and O’Reilly, 2003; Mayes et al., 2007). Here, an episode is some unique prior event defined by arbitrarily-associated elements, and the remembered details are present at the time of encoding but absent at the time of retrieval. Some have argued for implicit influences on, or components of, recollection (e.g., Turk-Browne et al., 2006; Sheldon and Moscovitch, 2010; Taylor and Henson, 2012; Taylor et al., 2013). We do not contest these claims, but here we focus on the canonical aspects of recollection in which the remembered details are brought to mind explicitly. 3 Recollection is frequently contrasted with a less precise, more automatic signal-strength process, often termed familiarity (Mandler et al., 1969; Juola et al., 1971; Anderson and Bower, 1972; Atkinson and Juola, 1973; Mandler, 1980; Tulving, 1985). Familiarity – the subjective sense that an item or situation has been encountered before – has been proposed to depend on a continuous memory strength signal (Kintsch, 1967; Juola et al., 1971). The value of this signal for a given item is augmented by learning when the item is encountered. Familiarity therefore provides a basis for judging prior occurrence, since previously encountered items on average possess higher signal strength than novel items. The contrast between recollection and familiarity is a popular process-based distinction in memory research. For example, “Dual-Process” theories of recognition memory assume that recollection and familiarity jointly underlie judgements of prior occurrence, and have inspired empirical frameworks for dissociating the relative contributions of the two processes (Jacoby, 1991; Yonelinas, 1994; Yonelinas and Jacoby, 1994). Although some recent studies have questioned the strength of the evidence for dual process models (Wixted, 2007; Dunn, 2008; Ratcliff and Starns, 2009; Jang et al., 2011; Rotello, 2017), the dual-process framework has been an influential and successful approach within cognitive neuroscience for explaining how distinct brain regions contribute to remembering (e.g., Aggleton and Brown, 1999, 2006; Brown and Aggleton, 2001; Meeter et al., 2005; Eichenbaum et al., 2007; Montaldi and Mayes, 2010; Webster et al., 2013; Wang et al., 2018). In these models, which emphasize the well-documented role of medial temporal lobe (MTL) structures in declarative memory, recollection is typically ascribed to the hippocampus, or a network including the hippocampus, whereas familiarity is associated with distinct neocortical sites such perirhinal cortex. Here, we set aside the debate over whether recognition memory draws on one or two processes (for a discussion of this see Rotello