We argue here that memory

We argue here that memory is far from unitary. Improvements in the precision of lesion studies (e.g., Heuer and Bachevalier, 2011; Pascalis et al., 2009) and imaging in human adults (e.g., Bakker et al., 2008; Ranganath, 2010; Staresina et al., 2011) demonstrate that MTL supports diverse forms of memory. For instance, visual-paired comparison (VPC), which reveals object memory in a preference for a novel object over a familiar one after a delay, was long thought hippocampally mediated (Heuer and Bachevalier, 2011). But, human infants exhibit robust performance on this task with neonates exhibiting a novelty effect after a 2-min delay (Pascalis and de Schonen, 1994), 3 month olds sustaining a delay of 24h (Pascalis et al., 1998) and 6 month olds a delay of 2 weeks (Fagan, 1973). This was taken at the time as evidence of hippocampal-mediated memory function in infancy (Hayne, 2004; Robinson and Pascalis, 2004). However, recent studies in nonhuman purchase MM-102 (Heuer and Bachevalier, 2011; Zeamer et al., 2010, 2015) with ablations targeted to specific MTL structures (e.g., hippocampus or PRC exclusively) reveal that object memory is heavily supported by the PRC (see Jabés and Nelson, 2015 for the proposal that some function could be supported in the subiculum of the hippocampus). Although hippocampus acts as an index, binding the elements of an event (e.g., object, scene) so they can be recognized together or separately (Brown and Aggleton, 2001; Davachi, 2006; Eichenbaum et al., 1994), the parahippocampal region supports memory in a unitized, or fused form, such that elements of events cannot be retrieved separately or recognized in new contexts (Graf and Schacter, 1989; Quamme et al., 2007). Given the underdevelopment of the trisynaptic circuit in infancy and rapid rates of neurogenesis in the DG that may impede retention (Josselyn and Frankland, 2012), the functions of DG pattern separation and CA3 pattern completion are not expected to be available until after infancy as evidenced by the protracted development of hippocampal function in early and middle childhood (e.g., Ghetti and Bunge, 2012; Ofen, 2012; Olson and Newcombe, 2014). As such, the late emergence of the trisynaptic circuit has ramifications for views of memory development. A few examples from the literature help to make this point.
Emergence of a hippocampal signature of memory function The integrity of hippocampal function is apparent after sleep-dependent delays in adults, and the mechanisms driving sleep-dependent memory consolidation can help guide predictions for similar developmental discontinuity in infant\'s long-term consolidation. Active Systems Consolidation (Diekelmann and Born, 2010), a prominent theory of sleep consolidation, based on complementary learning systems theory (McClelland et al., 1995) assumes that information is simultaneously encoded in the cortex and hippocampus during learning with hippocampus rapidly forming indices to cortex that provide a unique spatial and temporal context for later retrieval. In contrast, memories gradually integrate in cortex through repeated encodings and/or through sleep. In adult sleep three types of synchronized brain oscillations integrate memory into cortical stores (Diekelmann and Born, 2010; Moelle et al., 2002): high frequency, synchronous sharp-wave ripples reflecting neural replay of awake experience (Wilson and McNaughton, 1994) arise in CA3 and CA1 pyramidal cells (Chrobak and Buzsaki, 1994); sleep spindles, short high-frequency (9–15Hz), thalamo-cortical oscillations reflect communication between brain regions (Anders et al., 1971); and, slow waves, high amplitude, low frequency 1–4.5Hz oscillations originating in neocortex coordinate the activity of sharp-wave ripples and spindles (Coons and Guilleminault, 1982; Moelle et al., 2002). These synchronized oscillations are thought to reactivate hippocampal–cortical connections repeatedly during sleep, thus contributing to cortical strengthening and consolidation. Sleep spindles and slow wave activity correlate with memory retention in preschool age children and adults (e.g., Kurdziel et al., 2013; Tamminen et al., 2010). It is thus through sleep that hippocampal circuitry may support memory retrieval based on a single learning experience. Although sharp-wave ripples are one of the earliest oscillations to occur in development (Buzsaki, 2006), we argue that there cannot be mature CA1 replay and active systems consolidation until connectivity between CA3 and CA1 is sufficiently mature for the sharp-wave ripple activity originating in CA3 to propagate to CA1. Although rudimentary CA1 activity may propagate to cortex during infancy oscillations between hippocampus and cortex may be immature as reflected by the fact that children do not exhibit mature default network activity, thought to reflect intrinsic connectivity of the hippocampus with other memory systems, until about 2 years of age (Gao et al., 2009). Although basic trisynaptic circuitry is still forming before 24 months (Seress and Ábrahám, 2008), we propose that it may begin to support functional neural replay with sharp-wave ripple propagation to cortex by 18–24 months. Our proposal is supported by vastly different behavioral outcomes for sleep in infants and toddlers as we outline here.