CommentaryDoes assimilation into schemas involve systems or cellular consolidation? It’s not just time
Introduction
How does new information become incorporated into relevant frameworks of existing knowledge? What system and cellular mechanisms are involved in assimilating new information? The recent study of Tse et al. (2007), on which Rudy and Sutherland (2008) make interesting comments about the relative importance of systems and cellular consolidation, addresses this issue in the context of paired-associate learning. Using a paradigm in which rats were trained to use different flavors of food as cues to retrieve an associated spatial memory, we showed that after gradual learning (over several weeks) of a “schema” consisting of several paired-associates (PAs) involving spatial attributes, new PAs could be encoded, stored and consolidated in a single trial. Even though the task is hippocampal-dependent in the sense that new learning is blocked by lesions restricted to the hippocampus, we also observed that lesions given as soon as 48 h after the training of new PAs had no effect on subsequent memory. Lesions given 3 h after training blocked later memory. The implication seems to be that the encoding, storage and/or consolidation of new PAs is radically enhanced by prior knowledge and that systems consolidation of such information into cortex can occur much faster than has previously been observed.
Section snippets
Disruptive side-effects?
Rudy and Sutherland (2008) wonder, however, whether such unusually fast independence from the need for hippocampal processing during retrieval is really a consequence of rapid systems consolidation, or may reflect some unusual feature of our protocols. They re-plot aspects of our data for clarity, but our text may have misled them and other readers into thinking that we used a 24 h time-point for making lesions after new encoding. In fact, all lesions were either 3 or 48 h after the training of
The concept of hippocampal-dependence
It is important to stress that there are several different senses in which the learning of flavor-place PAs in this task can be said to be “hippocampal-dependent”, but other senses in which this description may seem misleading. First, the initial learning of naïve animals is impaired by hippocampal lesions that are made at the start of training (Tse et al., Fig. 1). Second, the learning of a new paired-associate schema in a new context by test-experienced animals is impaired by such lesions
Differential predictions
We have naturally wondered if there are distinct predictions that could be made based on Rudy and Sutherland’s “disruptive side-effects” and our “rapid systems-consolidation” perspectives. In our view, the key may be to finesse the side-effects of neurotoxic lesions by the alternative procedure of neural inactivation through AMPA receptor antagonists (such as CNQX), GABA agonists (such as muscimol), or even drugs that enable fast synaptic transmission but block plasticity (such as NMDA
Conclusions
While we disagree that the available data is consistent with Rudy and Sutherland’s (2008) alternative interpretation of our study, their commentary has been valuable in helping us to identify what we believe could be worthwhile follow-up experiments and in focusing on certain puzzling features of systems consolidation. Our stance, contrary to the sub-title of their piece, is that it is not “time that tells” as the defining feature of this memory process; it is the necessity for network
Acknowledgments
This commentary reflects work done under the auspices of an MRC Programme Grant and a Royal Society/Wolfson Award to R.G.M.M.
References (14)
On the use of ibotenic acid to lesion selectively different components of the hippocampal formation
Journal of Neuroscience Methods
(1989)- et al.
Is it systems or cellular consolidation? Time will tell. An alternative interpretation of the Morris Group’s recent Science Paper
Neurobiology of Learning and Memory
(2008) - et al.
Piloting and dead-reckoning dissociated by fimbria-fornix lesions in a rat food-carrying task
Behavioral Brain Research
(1997) - et al.
Neural systems underlying episodic memory: Insights from animal research
Philosophical Transactions of the Royal Society of London Series B
(2001) - et al.
Hippocampal lesions halve immediate–early gene production counts in retrosplenial cortex: Distal dysfunctions in a spatial memory system
European Journal of Neuroscience
(2007) - et al.
The effects of intrahippocampal ibotenic acid and their blockade by (−)2-amino-7-phosphonoheptanoic acid: Morphological and electroencephalographical analysis
Experimental Brain Research
(1983) - et al.
Multiple color optical activation, silencing and desynchronisation of neural activity with single-spike temporal resolution
PLoS One
(2007)
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2019, Developmental Cognitive NeuroscienceCitation Excerpt :Another possibility is that the maturation of the semantic network in the neocortex may still be under construction for the children compared to young adults. Schema memory research proposes faster assimilation of new information if there is an existing schema or prior knowledge related to the novel information (Bartlett, 1932; Tse et al., 2008, 2007; van Kesteren et al., 2014, 2012). Adults may have more well-established semantic schemata than children, and thus the pMTG may be more developed in adults than in children, facilitating the integration of novel words.
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2018, Neurobiology of Learning and MemoryCitation Excerpt :Some interactions among attributes aid in identifying the neural correlates that subserve critical interactions. For example, the interaction between sensory-perceptual attributes and the spatial attribute provide for the long-term memory representation of a spatial cognitive map or spatial schemas (Kesner, 2013c; Tse et al., 2007, 2008). It is suggested that the posterior parietal cortex (PPC) in rats represents the key neural substrate for the spatial component of the knowledge-based memory system.
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2015, Neurobiology of Learning and MemoryCitation Excerpt :The authors of that study, and some subsequent commentators, interpreted the data as evidence of rapid systems level consolidation in rats (Squire, 2007). Others, however, suggested that their results could be due to a slow cellular consolidation process instead (Rudy & Sutherland, 2008), especially in view of the disruptive effect of the neurotoxins used in the study to disable the hippocampus, although the authors reject this suggestion (Tse et al., 2008). Our human data, for which no hippocampal lesions were used, tentatively support the systems consolidation hypothesis; we cannot rule out a slow cellular consolidation process in this case, but it seems unlikely given the timeframe and ample evidence for systems level consolidation in humans over similar time periods (Durrant, Cairney, & Lewis, 2013; Rasch & Born, 2013; Takashima et al., 2006).
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2012, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Furthermore, flexibility to adjust abstract knowledge requires new learning and is hippocampus dependent. As a consequence of these observations it has been suggested that systems consolidation might not so much be about time but about the need for specific changes, i.e. cortico-cortical rewiring or synaptic modification (Tse et al., 2008). In support of this idea learning of information in the presence of a schema is accompanied by up-regulation of immediate early genes (IEG) in the mPFC (Tse et al., 2011).
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These authors contributed equally to this work.