Pattern separation, completion, and categorisation in the hippocampus and neocortex

“As the first stage in this pathway, the dentate gyrus is thought to separate entorhinal input patterns prior to memory storage in the hippocampus (Marr, 1971; McNaughton and Morris, 1987; Yassa and Stark, 2011; Schmidt et al., 2012; Knierim and Neunuebel, 2016; Rolls, 2016).”

“For recall, the hippocampal output can be thought of as a pointer to neocortical neurons via which memories can be called by using the backprojection pathways (Kesner and Rolls 2015; Rolls 2016a).”

“Importantly, the LC-CA3 and BA-CA1 pathways earlier triggered by rapid low-road processing of the GS, are R.D. Webler et al. Neuroscience and Biobehavioral Reviews 128 (2021) 421–436 proposed to increase the neural gain in CA3/CA1-based pattern completion circuits with the effect of predisposing the hippocampus toward…”

“…with each other) receive taste, somatosensory, olfactory, visual, and auditory inputs that are needed to build the reward and punishment value representations that are found in these regions but much less in the preceding cortical areas that provide these inputs (Rolls, 2016a, 2019a, 2019c, 2021a).”

“Results show that successful associative recognition (AR) yields enhanced event-specific reinstatement of encoding patterns compared to non-associative item recognition (IR).”

“Importantly, the CA3-DG region has been shown to support the information binding necessary to support relational memory and ensure successful performance in the administered task (Daugherty et al., 2017; Johnston et al., 2016; Rolls, 2016; Yassa & Stark, 2011).”

“CA3 neurons are highly-interconnected, a feature proposed to facilitate pattern completion and promote the retrieval of encoding related ensembles, which can then be conveyed to area CA1 (Marr, 1971; Montgomery & Buzsaki, 2007; Nakazawa et al., 2002; Norman & O’Reilly, 2003; O’Reilly & McClelland, 1994; Rolls, 2016; T…”

“…recognition, and a highly developed eye movement control system to bring the fovea to objects, using mechanisms described elsewhere (Rolls, 2012; Rolls, 2016a; Rolls, 2021a; Rolls, 2021f; Rolls, Aggelopoulos, & Zheng, 2003; Rolls, Deco, et al., 2022b; Rolls, Deco, et al., 2022c; Rolls & Webb,…”

“In this regard, volumetry of the sub fi elds may be a proxy for cumulative microstructural changes, such as neurogenesis and synaptic pruning — the putative neural basis of associative memory binding and reconstitution (Johnston et al., 2016; Rolls, 2016).”

“Neurogenesis in the hippocampal formation, one of the most important brain regions involved in pattern separation/completion and memory formation (Rolls, 2016), is severely disrupted in fetuses with DS (Contestabile et al.”

“(2) To test the effects of temporal structure of the excitatory drive (Supplementary Fig.”

“The hippocampus (particularly the trisynaptic loop formed by DG–CA3–CA1) is implicated in pattern separation/completion processes necessary to disambiguate similar stimuli (Norman and O’Reilly, 2003; Rolls, 2016).”

“This is a decorrelation or orthogonalization process, which is sometimes referred to as pattern separation, and which helps to make the transmission and storage of information have a high capacity (Marr, 1971; McNaughton & Morris, 1987; Rolls, 1987, 1989a, 2016b; Treves & Rolls, 1992).”

“…and this is how it is proposed that episodic memory in primates including humans is implemented, for it prototypically involves remembering and later recalling where people or objects have been seen in the spatial environment (Rolls, 2010, 2013a, 2013b, 2016, 2018, 2021a; Kesner & Rolls, 2015).”

“…effect of diluted connectivity in competitive networks such as the dentate granule cells, because this helps different neurons to fire differently to different inputs even before associative synaptic modification onto high firing rate neurons during the competitive learning (Rolls, 2016a, 2023c).”

“According to these models, exposure to part of a past experience leads to recurrent connectivity in the hippocampal CA3 subfield, retrieving the conjunctive representation of the entire event (Guzowski, Knierim, & Moser, 2004; Rolls, 2016).”

“Pattern separation is thought to accomplish this (e.g., Hunsaker & Kesner, 2013; Rolls, 2010, 2016).”

“…a balance between the competing processes of pattern separation and pattern completion within the dentate gyrus-CA3 network (McNaughton and Morris, 1987; Treves and Rolls, 1994; McClelland et al., 1995; O’Reilly and Norman, 2002; Norman and O’Reilly, 2003; Yassa and Stark, 2011; Rolls, 2013, 2015).”

“This reinstatement may enhance processes such as pattern completion (Staresina et al., 2012, 2016; Tompary et al., 2016) where similar network level inputs are transmitted to regions reconstructing the pattern of activity laid down at encoding, such as is thought to occur in hippocampal area CA3 (Norman and O’Reilly,…”

“Classical models of the CA3 circuit suggest that activation of mossy fiber synapses results in the induction of synaptic plasticity in RC CA3-CA3 synapses ( 10 – 12 , 122 ).”

“It is widely acknowledged that the hippocampus and its different subfields play a crucial role in memory processes [Horner and Doeller, 2017; Rolls, 2016].”

“CA3 then becomes the key site of the conflict (1) between encoding of such similar perceptual inputs (pattern separation) and retrieval of stored representations held in the autoassociative network of CA3 via its recurrent collateral circuitry (pattern completion) (2).”

“…of hippocampal subfields to pattern separation: Computational models assume that the DG performs pattern separation by means of sparse coding of neural activity from the entorhinal cortex (EC) to CA3 thereby decorrelating overlapping neural assemblies (Rolls, 2016; Treves & Rolls, 1994).”

“…Moreno et al., 2016; Moser et al., 2017; Moser et al., 2008; O’Keefe, 1976; O’Keefe and Dostrovsky, 1971; O’Keefe and Recce, 1993; Okuyama et al., 2016; Rolls, 2016; Rolls et al., 2005; Rolls and Wirth, 2018; Roy et al., 2017; Sirota and Buzsáki, 2005; Squire et al., 2015; Terrazas, 2005;…”

“A key difference is that parts of scenes cannot be moved with respect to other parts of scenes without creating a new spatial scene (Rolls, 2016a; Rolls, 2021).”

“Critically, hippocampal subfields differentially participate in these processes (Montaldi & Mayes, 2010; Neunuebel & Knierim, 2014; O ’ Reilly & McClelland, 1994; Rolls, 2016).”

“Notably, neural reinstatement depends on the hippocampus because CA3 pyramidal cells have extensive synaptic connections which enable previous patterns of neural activity to be easily reinstated during retrieval (Marr, 1971; Norman & O’Reilly, 2003; Rolls, 2016).”

“On a neural level, computational models suggest that within the hippocampal network, the DG performs pattern separation by a decorrelation of overlapping neural assemblies at encoding (Treves and Rolls, 1994; Rolls, 2016).”

“These analyses emphasize the utility of having a sparse representation in the hippocampus, for sparse distributed representations increase the number of different memories that can be stored (Treves & Rolls, 1991a), essential for an episodic memory (Rolls, 2010, 2016b, 2018, 2023a).”

“The DG is thought to contribute to the formation of new episodic memories, novelty, and pattern separation (Bakker et al., 2008; Goodrich-Hunsaker et al., 2008; Rolls, 2016; Leutgeb et al., 2007).”

“Neuronal populations in the hippocampal CA3 subfield are part of the mammalian brain circuit 88 that is essential for spatial navigation, memory formation, and cognition (Kesner, 2007; Hartley 89 et al., 2013; Rolls, 2016; Rebola et al., 2017; Hainmueller and Bartos, 2018).”

“A fundamental aspect of many cognitive activities as perception, working memory and LTM, is the ability to discern subtle changes in the environment, often denoted as pattern separation (78).”

“25 sparseness of representations in different parts of the human hippocampal system or between the hippocampus and neocortex [1], but in macaques it has been shown that representations in the hippocampus are more sparse than in three neocortical areas [6], in line with the pattern separation hypothesis [3,4].”

“LTD mechanisms would need to occur in order to erase some details of older memories (form structured/gist‐ like memories) and fit the network capacity for encoding and recalling (as part of learning) new information (Rolls, 2016, 2017).”

“These findings suggest that both category learning and category generalization should depend on the hippocampus (Rolls, 2016).”

“…retrieval of extinguished memory is now established (Milad, Wright, et al., 2007), the specific role of subfields is still being investigated (Rolls, 2016); and differential roles have been proposed both in humans (Dimsdale-Zucker, Ritchey, Ekstrom, Yonelinas, & Ranganath, 2018) and in…”

“The numbers of neurons in different parts of the hippocampal trisynaptic circuit in humans [87] are shown in (a), and indicate very many dentate granule cells, consistent with expansion encoding and the production of sparse uncorrelated representations prior to CA3 [88,89].”

“This has many implications for understanding attentional effects to affective value not only on taste, but also on other sensory stimuli (Ge et al., 2012; Luo et al., 2013; Rolls, 2013b, 2014, 2016c).”

“Neurogenesis, dendrization, and pruning within the DG and CA3 are considered to underlie information binding and reconstitution in relational memory (Johnston, Shtrahman, Parylak, Gonçalves, & Gage, 2016; Rolls, 2016).”

“Herewe have demonstrated that themTOR/p70S6Kpathway inCA3pyramidal neurons is activated during the encoding of an inhibitory avoidance memory, confirming the hypothesis that CA3 is especially needed in rapid one trial place memory (Rolls, 2016).”

“We focused on the MST’s lure discrimination index (LDI), which tests object recognition memory using highly similar lure items in an effort to tax the hippocampal function known as pattern separation (Rolls, 2016; Yassa & Stark, 2011).”

“…attribute pattern separation to hippocampus (specifically the DG subfield), with limited roles for adjacent medial temporal regions (e.g., memory reinstatement, learning statistical regularities, visual feature extraction; Norman, 2010; O'Reilly, Bhattacharyya, Howard, & Ketz, 2014; Rolls, 2016).”

“32 ).”

“…orthogonalization of inputs from parahippocampal cortical regions, minimizing interference (McNaughton and Morris, 1987; Treves and Rolls, 1992; O’Reilly and McClelland, 1994; Rolls and Kesner, 2006; Treves et al., 2008; Yassa and Stark, 2011; Santoro, 2013; Kesner and Rolls, 2015; Rolls, 2016).”

“…Montreal, Canada, H3A 1G1 2020 Informa UK Limited, trading as Taylor & Francis Group been linked to the functioning of the dentate gyrus of the hippocampus (Rolls, 2016), which is a hippocampal subfield that is particularly sensitive to the effects of acute stress (McEwen, Nasca, & Gray, 2016).”

“…1999; Hasselmo & Wyble, 1997; Lever et al., 2010; Levy, 1989; Lisman & Otmakhova, 2001; Vago & Kesner, 2008), pattern completion (Cheng, 2013; Rolls, 2016), processing temporal information (Gilbert et al., 2001; Mankin et al., 2012; Rolls & Kesner, 2006), transforming CA3 representations for…”

“Pattern completion is an inherent property of an autoassociation or attractor network such as the CA3 recurrent collateral system is believed to be (Rolls, 2008, 2016a), and there is also therefore great interest in the mechanisms for pattern completion in the hippocampal system.”

“Important to learning specific episodes are pattern separation that discriminates between similar memories through the reduction of representational similarity, and pattern completion that retrieves linked associations among co-occurring elements (Marr, 1971; Norman & O’Reilly, 2003; Rolls, 2016).”

“…the left and right hippocampus was detected, as well as functional lateralization; for example, the right hippocampus may be devoted to episodic memories with spatial and visual components, whereas the left hippocampus may be devoted to memories with verbal or linguistic components (Rolls, 2016).”

“Given that there is one principal excitatory neuron type in the neocortex, the pyramidal cell (Rolls 2016a), the research described here is conceptually an important advance, for it shows that all these types of computation can be performed with one type of single neuron with the connections and…”

“…items bothshowedenhancedrecognition(CS + >CS − )butdivergedaccord-ing to the canonical memory systems of “ pattern completion ” and “ pattern separation, ” which are well documented across decades of memory research (Marr 1971; Rolls 2016) yet rarely studied in the context of human fear memory.”

“Two generic computations of funda-147 mental theoretical relevance ( 37 ) are pattern completion, which allows accurate retrieval or generalization from partial inputs, and pattern separation, which improves discrimination of similar inputs ( 4,35,37,44 ).”

“As a preprocessor for the CA3, the principal GCs perform pattern separation on the input patterns from the EC by sparsifying and orthogonalizing them, and send the pattern-separated outputs to the pyramidal cells in the CA3 through the mossy fibers (MFs) (Treves and Rolls 1994; O’Reilly and McClelland 1994; Schmidt et…”