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Reconsolidation or re-association?

Published online by Cambridge University Press:  08 June 2015

Sue Llewellyn*
Affiliation:
Faculty of Humanities, University of Manchester, Manchester M15 6PB, United Kingdom. sue.llewellyn@manchester.ac.ukhttp://www.humanities.manchester.ac.uk

Abstract

The target article argues memory reconsolidation demonstrates how therapeutic change occurs, grounding psychotherapy in brain science. However, consolidation has become an ambiguous term, a disadvantage applying also to its derivative – reconsolidation. The concept of re-association (involving active association between memories during rapid eye movement [REM] dreams followed by indexation and network junction instantiation during non-rapid eye movement [NREM] periods) brings greater specificity and explanatory power to the possible brain correlates of therapeutic change.

Type
Open Peer Commentary
Copyright
Copyright © Cambridge University Press 2015 

Reconsolidation and consolidation have various connotations (Llewellyn Reference Llewellyn2013b): (re)stabilization; (re)strengthening; (re)storage; and (re)resistance to interference. Although consolidation originally implied progressive stabilization (Müller & Pilzecker Reference Müller and Pilzecker1900), dynamic memory reorganization is now also subsumed under (re)consolidation. Indeed, Stickgold and Walker (Reference Stickgold and Walker2005) suggest consolidation and reconsolidation probably reflect memory organization and reorganization. (Re)consolidation also confounds two distinct neurobiological levels: first, synaptic, through Hebbian plasticity (Hebb Reference Hebb1949) and long-term potentiation (Bliss & Collingridge Reference Bliss and Collingridge1993); and second, system, to integrate recent memories with remote ones (Dudai Reference Dudai2004; Frankland & Bontempi Reference Frankland and Bontempi2005; Tamminen et al. Reference Tamminen, Payne, Stickgold, Wamsley and Gaskell2010). Given this ambiguity, (re)consolidation may obscure rather than enhance understanding.

Long-term episodic memories are represented in cortical networks (Fuster Reference Fuster1997; Reference Fuster1999; Reference Fuster2006; Reference Fuster2009). If therapeutic change impacts on long-term memory, then memory networks must be modified in some way. The exploration of a remote disturbing memory during therapy creates a new memory that, we hope, acquires some positive connotations. The reconsolidation concept implies plasticity and synaptic weight changes (the first level referred to above), through new more positive associations within the old disturbing memory network pathway. But reconsolidation leaves the second, system integration level, an open question: How is this recent memory of exploring the old traumatic memory within therapy integrated with other memories, resulting in associations between different memory networks.

Integration and segregation are fundamental to cortical network organization (Tononi et al. Reference Tononi, Sporns and Edelman1994; Zeki Reference Zeki1978; Zeki & Shipp Reference Zeki and Shipp1988). Networks intersect abundantly; some intersections are omnidirectional junctions (Fuster Reference Fuster1997; Reference Fuster1999). Neurons at an omnidirectional junction collectively define the meaning or significance of the several memory pathways that meet there (Buzsáki Reference Buzsáki2005). Consequently, therapeutic change may involve: first, introducing some positive associations into the memory pathway and, second, integrating this memory to others with positive connotations at a new omnidirectional junction that defines their shared meaning. Indeed, the latter may rely on the former.

Re-association, through new junction instantiation, would involve dynamic modification to the cortical network connectivity matrix. Memory representation most likely uses structural plasticity (or re-wiring) alongside the better recognized, synaptic weight changes (Chklovskii et al. Reference Chklovskii, Mel and Svoboda2004; Sporns et al. Reference Sporns, Chialvo, Kaiser and Hilgetag2004). Re-wiring implies memory network reorganization – the latter is known to occur during sleep, enabling flexible generalization from several memories (Ellenbogen et al. Reference Ellenbogen, Hu, Payne, Titone and Walker2007; Wagner et al. Reference Wagner, Gais, Haider, Verleger and Born2004), congruent with making associations between different memory networks.

During slow wave sleep, effective corticocortical connectivity breaks down (Massimini et al. Reference Massimini, Ferrarelli, Huber, Esser, Singh and Tononi2005; Spoormaker et al. Reference Spoormaker, Schröter, Gleiser, Andrade, Dresler, Wehrle, Sämann and Czisch2010), reducing cortical integration (Esser et al. Reference Esser, Hill and Tononi2009) and, possibly, reflecting some network reorganization to enable new integrative memory associations in later sleep stages. In the REM-rich second half of the night, hippocampal associational function may identify the collective significance of several memories, portraying this meaning as an associative REM dream image, and enabling a new integrative omnidirectional junction to be instantiated in cortical networks at a subsequent NREM Stage 2 period (Llewellyn Reference Llewellyn2013a).

These processes may serve both emotional memory encoding (the identification of meaningful associations) and retrieval (the same associations trigger the memory) (cf. Tulving & Thomson Reference Tulving and Thomson1973). Indeed, in accordance with the indexing theory of hippocampal function (Hirsh Reference Hirsh1974; Teyler & DiScenna Reference Teyler and DiScenna1986; Teyler & Rudy Reference Teyler and Rudy2007), REM dream scenes may be retained as unconscious hippocampal indices that match the omnidirectional junctions where several cortical network memories meet and can be found (Llewellyn Reference Llewellyn2013a). Physiologically, the temporal coincidence of hippocampal sharp wave-ripples with neocortical spindles signals network integration (Tamminen et al, Reference Tamminen, Payne, Stickgold, Wamsley and Gaskell2010) and may reflect indexation and NREM junction instantiation respectively.

The configuration of conscious, segregated episodic memory pathways whose collective meaning is represented at integrative, unconscious omnidirectional junctions may resonate with conscious and unconscious memory. As discussed in the target article, the unconscious has an adaptive, evaluative, processing function (Gazzaniga Reference Gazzaniga1998), congruent with identifying the meaning of several associated memories. Contemporarily, “meaning” has abstract definition, the expression of an idea in language but, as pointed out in the target article, “meaning” can imply concrete, personal significance. REM dreams may identify the collective significance of several associated memories for the needs, desires, or goals of the dreamer, having either broadly positive (if congruent with needs, etc.) or negative (if not) emotional impact. Emotional arousal in REM dreams would result from revealing the significance of related experiences for needs and so forth, and it may explain why emotional arousal signals successful therapy.

If an old, disturbing memory is highly traumatic, especially if perceived as life threatening at the time, it may be too negative to be associated with other memories in a REM dream. Normally REM dreams portray elements of several memories (Fosse et al. Reference Fosse, Fosse, Hobson and Stickgold2003; Hartmann Reference Hartmann1996; Hobson Reference Hobson1988, pp. 36–38; Walker & Stickgold Reference Walker and Stickgold2010), consistent with an associational function. When a memory is replayed in entirety in nightmares, as observed in post-traumatic stress disorder (PTSD; Nielsen & Stenstrom Reference Nielsen and Stenstrom2005) this may reflect a failure of association, resulting in a lack of integration with other memories at an omnidirectional junction. The memory would be retained in the cortex but not fully incorporated – as an assimilated life experience – in the integrative network. Therapy that introduces some positive associations into the old memory may be successful in enabling later association with others in a REM dream.

Re-association offers a more nuanced and dynamic account of the neural substrates of psychotherapy than the over-stretched reconsolidation concept does. If life experience has failed but therapy succeeds in introducing more positive associations into a traumatic memory, two more stages may integrate this memory into cortical networks. First, this new recent memory is actively and consciously associated with other more remote memories in a REM dream scene. Second, this REM dream scene is retained as an unconscious hippocampal index and instantiated during NREM as a new unconscious omnidirectional junction in episodic cortical networks. This two-stage process shows how re-association involves indexation and instantiation also. It also explains how unconscious memory influences thought and action because unconscious associations are processed on episodic memory retrieval after matching between hippocampal indices and omnidirectional cortical junctions.

On this account, “the unconscious” is not localized but dispersed throughout the cortex at omnidirectional junctions, which, after the association of several episodic memories in REM dreams, represent their collective meaning. Free association to the dream may uncover these memories and their shared significance. Freud (Reference Freud and Crick1899/1999) famously declared, “The interpretation of dreams is the royal road to a knowledge of the unconscious activities of the mind.” On this version of relevant neural events, retained dreams are the unconscious, so he has to be right!

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