A spontaneous neural replay account for involuntary autobiographical memories and déjà vu experiences

Abstract

Barzykowski and Moulin argue both involuntary autobiographical memories and déjà vu experiences rely on the same involuntary memory retrieval processes but their underlying neurological basis remains unclear. We propose spontaneous neural replay in the default mode network (DMN) and hippocampus as the basis for involuntary autobiographical memories, whereas for déjà vu experiences such transient activation is limited to the DMN.

Involuntary autobiographical memories (IAMs) and déjà vu experiences are not uncommon in our daily life. Both involve memory recall that occur spontaneously without any deliberate/conscious intention to recall them. Barzykowski and Moulin (B&M) posit both IAMs and déjà vu experiences result from the same involuntary memory retrieval processes, while claiming that IAMs are distinct because of their explicit accessibility to the retrieved memory content. However, the neurological basis of these two phenomena remains unclear in the target article. In this commentary, we propose spontaneous neural replay in the hippocampus and default mode network (DMN) as the basis for experiencing IAMs, whereas for déjà vu experiences such transient activation is limited to the DMN.

Spontaneous neural replay refers to spontaneously generated reactivation of neural activity and configurations related to past experiences (Schuck & Niv, 2019). It occurs preferentially during brief bursts (~30–100 ms) of high-frequency (~200 Hz) neural firing known as sharp-wave ripples (Dickey et al., 2022). Such spontaneous brain activity occurs as a result of intrinsic brain dynamics as well as cued reactivation by sensory stimuli (Liu, Nour, Schuck, Behrens, & Dolan, 2022). Spontaneous neural replay is a critical process supporting memory consolidation (Deuker et al., 2013) and memory retrieval (Vaz, Wittig, Inati, & Zaghloul, 2020). Spontaneous neural replay has been noted to occur in the hippocampal (Gillespie et al., 2021) and the neocortical memory systems (e.g., DMN nodes; Higgins et al., 2021). Hippocampus and DMN nodes (e.g., medial prefrontal cortex [mPFC]; posterior cingulate cortex [PCC]) have been implicated in supporting a range of memory-related functions including autobiographical memory retrieval (Cabeza & St Jacques, 2007; Philippi, Tranel, Duff, & Rudrauf, 2015).

According to the cascaded memory systems model (Kaefer, Stella, McNaughton, & Battaglia, 2022), spontaneous neural replay in the DMN can be independently triggered in the absence of corresponding hippocampal replay. Transient activation limited to DMN and its propagation to areas downstream of DMN (e.g., unimodal sensory cortices) correspond to reactivation of only factorized feature representations that make up a memory (Kaefer et al., 2022). Such features may involve various attributes or details of a memory's content. Kaefer et al. (2022) also claim that hippocampal replay in conjunction with spontaneous neural replay in DMN and its downstream propagation to primary sensory cortices are essential to the retrieval of a complete memory. Being a critical brain region for memory encoding (Scoville & Milner, 1957), hippocampus is considered to generate and store highest-order memory representations (Kaefer et al., 2022). These highest-order memory representations could be viewed as index codes that support the binding of contextual details of a memory (Simons, Ritchey, & Fernyhough, 2022). Therefore, hippocampal replay reactivates the highest-order memory index codes necessary for binding or integrating the factorized feature representations of a memory into a cohesive whole (Goode, Tanaka, Sahay, & McHugh, 2020).

Inspired by the cascaded memory systems model (Kaefer et al., 2022), we propose spontaneous neural replay in the DMN occurring in the absence of hippocampal replay forms the neural basis of déjà vu (Fig. 1a). For déjà vu experiences, the memory retrieval process is incomplete and the memory contents are inaccessible because the memory representations spontaneously reactivated in the DMN are factorized and lack the highest-order memory index codes presumed to be generated and stored only in the hippocampus (Kaefer et al., 2022). Therefore, in the absence of hippocampal replay, the reactivated representations in the DMN are unable to be integrated into a complete autobiographical memory. Instead, transient activity in the DMN may correspond to reactivation of some stored features or attributes of an autobiographical memory, thereby evoking a vague sense of familiarity to specific features typical of déjà vu experiences. Complete memory retrieval of IAMs and access to their memory contents occur only when spontaneous neural replay occurs in both the hippocampus and DMN (Fig 1b). Reactivation of hippocampal highest-order memory index codes allows for the binding or integration of the various factorized feature representations reactivated in the DMN, resulting in a successful involuntary retrieval of an autobiographical memory with explicit accessibility to its contents.

Figure 1. The spontaneous neural replay account for (a) déjà vu experiences and (b) involuntary autobiographical memories (IAMs).

Further support to our spontaneous neural replay account comes from lesion studies. McCormick, Rosenthal, Miller, and Maguire (2018) found that patients with bilateral hippocampal damage could engage in spontaneous thinking but were unable to report contents of their spontaneous thoughts about their memories. This suggests hippocampus plays a critical role in the complete and successful retrieval of IAMs. Additionally, the earliest/preclinical stages of Alzheimer's disease (AD) are characterized by accumulation of extracellular β-amyloid primarily in DMN nodes such as PCC and mPFC which produces cell atrophy and disrupted functional connectivity in the DMN (Palmqvist et al., 2017). Such disruption to DMN in early AD has been associated with reductions in the rate of spontaneous thoughts about the past without impairing accessibility to their contents (Kvavilashvili, Niedźwieńska, Gilbert, & Markostamou, 2020; O'Callaghan, Shine, Lewis, Andrews-Hanna, & Irish, 2015). Taken together, disruption to hippocampus and DMN may impair distinct aspects (accessibility to memory contents vs. frequency of spontaneous recall) of involuntary retrieval of autobiographical memories.

Future studies are warranted to directly dissociate the contribution of hippocampus and DMN in spontaneous memory retrieval. It would be advantageous to examine spontaneous neural replay across cortical DMN nodes and subcortical structure of hippocampus by combining neuroimaging techniques that offer both high temporal and spatial resolutions (e.g., magnetoencephalography). In conclusion, we have implicated spontaneous neural replay in hippocampus and DMN as the neural basis for IAMs while transient activation limited to DMN supports déjà vu experiences. By highlighting the critical role of spontaneous neural replay in involuntary memory processes and how replay in different neural substrates contributes distinctly to involuntary retrieval, we offer a more nuanced neurocognitive perspective on how IAMs and déjà vu experiences differ.