The representational–hierarchical view of pattern separation: Not just hippocampus, not just space, not just memory?
Introduction
The importance of complex conjunctive representations for the resolution of ambiguity in lower-level representations has been a major focus of our research and that of others. Much work from several species and experimental approaches suggests that this principle of resolution of ambiguity via conjunctive representations has considerable explanatory power, particularly regarding how best to understand the effects of focal brain dysfunction (e.g., Barense et al., 2005, Barense et al., 2012, Bartko et al., 2007, Bussey and Saksida, 2002, Cowell et al., 2006, Cowell et al., 2010a, Graham et al., 2006, Lee, Buckley, et al., 2005, Lee, Bussey, et al., 2005, Lee and Rudebeck, 2010, McTighe et al., 2010). We have referred to this way of thinking about brain organization as the “representational–hierarchical” perspective (R–H) (e.g., Bussey and Saksida, 2002, Bussey and Saksida, 2005, Murray et al., 2007, Saksida and Bussey, 2010).
Recently there has been a great deal of interest in a process referred to as “Pattern Separation” (PS). PS has been defined as “… reducing interference among similar inputs by using non-overlapping representations…” (e.g., Reagh et al., 2014) and “…the ability of the network to reduce the overlap between similar input patterns before they are stored in order to reduce the probability of interference…” (Neunuebel & Knierim, 2014). Clearly the main principle of the R–H framework, the resolution of the “ambiguity” of lower level representations via the formation of unique conjunctive representations in higher level areas, is a strikingly similar idea to the above conceptions of PS. The present article is, therefore, aimed at researchers interested in PS, and explores the question: To the extent that researchers are interested in PS because it results in the formation of new, interference-reducing representations, what insights into PS might be offered by considering some of the conclusions resulting from R–H theory?
A quick word about the scope and aims of this review. R–H theory grew out of an interest in the functional relevance of processes and representational content in the brain. That is, what such processes and representational content do for us, in aspects of cognition such as memory and perception. The way to determine this is through empirical, causal behavioral experiments that measure cognition. Non-empirical approaches such as computational modeling have been hugely important in the area of PS (O’Reilly and McClelland, 1994, Rolls, 1987, Rolls, 1989, Rolls, 1990; Norman and O’Reilly, 2003, Rolls and Kesner, 2006, Treves and Rolls, 1994) and indeed, experiments testing the R–H view have been guided by computational modeling (e.g., Barense et al., 2012, Bartko et al., 2007, Cowell et al., 2006). But we must remember that these are models, and at some point experiments on real brains must be done. Correlational experimental approaches, particularly electrophysiology, have shed much light on PS at the cellular and network levels (e.g., Nakashiba et al., 2012, Knierim and Neunuebel, 2016), and focus on PS as a specific mechanism involving the transformation of an input representation to an output representation, in which the output is less correlated than the input (in line with computational models). However this process is of interest because of the representations thus formed and in particular their requirement for cognition (usually memory). Correlational approaches generally do not address this requirement. Additionally, correlational approaches have largely focussed on the hippocampus, whereas a main aim of what follows below is a suggestion that we need to consider other areas of the brain with respect to PS. Fully understanding any function of the brain cannot be accomplished by any single method alone, but requires converging, complementary approaches.
Furthermore, our focus in this article is the relevance to cognition of the result of processes such as PS, i.e., the representations that are formed from such processes. We will not, in this review, discuss how these representations are formed. For example, we will consider that such representations may be housed in the ventral visual stream, but not the way the formation of such representations might be related to the receptive fields of neurons. Comprehensive treatments of such issues, along with the properties of such representations (e.g., invariance), can be found in other sources such as Rolls (2016).
Insofar as PS can be considered to be a process of forming new representations that help resolve ambiguity, the results of experiments carried out under the auspices of R–H theory lead us to offer a number of possibly surprising hypotheses about PS, including:
- 1.
PS is fundamental to many aspects of cognition including perception; it is not just for memory.
- 2.
PS happens in many cortical regions, not just the hippocampus.
- 3.
PS happens for all stimulus material and not just ‘spatial’ or ‘episodic’ material. It happens for different types of representations, in the different regions and different levels throughout the “representational hierarchy”.
- 4.
The dentate gyrus (DG) is unlikely to maintain all levels of representation, and thus is not a truly domain-general pattern separator.
- 5.
PS – insofar as this term equates with the formation of interference-reducing conjunctive representations – may have much wider explanatory power for understanding the effects of brain dysfunction than previously suspected.
Below we provide a brief history and summary of R–H theory, with special emphasis on these particular conclusions regarding PS, and then return to these points.
Section snippets
The Representational–Hierarchical model: A brief history and summary
The R–H view was first presented in 1998 (Saksida & Bussey, 1998) and discussed in a review article in 1999 (Murray & Bussey, 1999). Eventually the first modeling and experimental studies testing the theory were published (Bussey and Saksida, 2002, Bussey et al., 2002, Bussey et al., 2003). Although R–H takes a broad view of cognition, initial studies focused on visual cognition, and in particular the issue of whether there are dedicated, anatomically segregated memory (Squire & Zola-Morgan,
What does any of this have to do with PS?
The relevance of R–H principles to PS is that all of the above and more can be explained by the formation of highly discriminable representations that resolve interference or ambiguity, which is thought to be the function of PS (see definitions above). This suggests that PS is a rather powerful process that happens in many parts of the brain, and may be a major player in many aspects of cognition.
It is worth taking a moment to focus on the last point above, the proposal that the hippocampus is
Concluding thoughts
To recap, the main points arising from this analysis are:
- 1.
PS is fundamental to many aspects of cognition including perception; it is not just for memory.
- 2.
PS happens in many cortical regions, not just the hippocampus.
- 3.
PS happens for all stimulus material and not just ‘spatial’ or ‘episodic’ material. It happens for different types of representations, in the different regions and different levels throughout the hierarchy.
- 4.
The DG is unlikely to maintain all levels of representation, so is not a
Acknowledgments
LMS and TJB were funded by Medical Research Council/Wellcome Trust grant 089703/Z/09/Z. BAK was funded by Gates Cambridge and the Natural Sciences and Engineering Research Council of Canada (NSERC).
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