Functional connectivity with the hippocampus during successful memory formation

Ranganath, Charan; Heller, Aaron S.; Cohen, Michael X; Brozinsky, Craig J.; Rissman, Jesse

doi:10.1002/hipo.20141

Cited by 202 publications

(155 citation statements)

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“…Our finding may thus reflect increased allocation of neural resources to integrative mnemonic processes. In agreement, a previous study showed enhanced hippocampal-neocortical connectivity during successful memory encoding (15). An interesting parameter, however, is the directionality of such interactions (38): If such interactions indeed promote integration into cortical-cortical networks, one would expect directional dominance toward the neocortex.…”

Section: Discussionsupporting

confidence: 86%

“…During encoding, neurons in medial prefrontal cortex (PFC) have been shown to exhibit unit activity that is phase locked to hippocampal theta oscillations (14). Moreover, functional connectivity between these regions as measured using functional MRI (fMRI) in humans has been shown to predict subsequent memory (15). Furthermore, there is evidence of postencoding reactivation of memory traces within similar circuits.…”

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confidence: 99%

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Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans

Kesteren

Fernández

Norris

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

420

313

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The hippocampus is thought to promote gradual incorporation of novel information into long-term memory by binding, reactivating, and strengthening distributed cortical-cortical connections. Recent studies implicate a key role in this process for hippocampally driven crosstalk with the (ventro)medial prefrontal cortex (vmPFC), which is proposed to become a central node in such representational networks over time. The existence of a relevant prior associative network, or schema, may moreover facilitate this process. Thus, hippocampalvmPFC crosstalk may support integration of new memories, particularly in the absence of a relevant prior schema. To address this issue, we used functional magnetic resonance imaging (fMRI) and prior schema manipulation to track hippocampal-vmPFC connectivity during encoding and postencoding rest. We manipulated prior schema knowledge by exposing 30 participants to the first part of a movie that was temporally scrambled for 15 participants. The next day, participants underwent fMRI while encoding the movie's final 15 min in original order and, subsequently, while resting. Schema knowledge and item recognition performance show that prior schema was successfully and selectively manipulated. Intersubject synchronization (ISS) and interregional partial correlation analyses furthermore show that stronger prior schema was associated with more vmPFC ISS and less hippocampal-vmPFC interregional connectivity during encoding. Notably, this connectivity pattern persisted during postencoding rest. These findings suggest that additional crosstalk between hippocampus and vmPFC is required to compensate for difficulty integrating novel information during encoding and provide tentative support for the notion that functionally relevant hippocampal-neocortical crosstalk persists during off-line periods after learning.declarative memory | memory consolidation | resting state | functional connectivity | functional MRI T he formation of long-term memory traces involves a gradual integration of newly acquired information into neocortical associative networks (1, 2). The hippocampus is thought to promote this process by binding, reactivating, and strengthening connections between distributed neocortical representations, thus gradually reducing hippocampal dependence of the memory trace (3-5). Recent findings, however, show a concomitant increase in dependence on the (ventral) medial prefrontal cortex (vmPFC) (6-9) that may develop rapidly depending on contextual factors (10). These findings suggest that the binding role of the hippocampus may be transferred to the vmPFC (6, 11, 12) and implicate hippocampal-neocortical interactions in early stages of long-term memory formation (13).Several lines of animal and human research suggest that coupling between these regions occurs at different stages of long-term memory formation. During encoding, neurons in medial prefrontal cortex (PFC) have been shown to exhibit unit activity that is phase locked to hippocampal theta oscillations (14). Moreover, functional connec...

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Section: Discussionsupporting

confidence: 86%

mentioning

confidence: 99%

Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans

Kesteren

Fernández

Norris

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

420

313

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“…This finding is also consistent with the results of a previous functional neuroimaging study, in which the MTL activity during successful encoding was functionally connected with the OFC and other cortical activity (Ranganath et al, 2005). Moreover, the OFC-MTL connection has been identified in human subjects using DTI (Powell et al, 2004).…”

Section: Functional Connectivity Between the Orbitofrontal And Medialsupporting

confidence: 91%

“…White matter connections between OFC and MTL have also been demonstrated using diffusion tensor imaging (DTI) in humans (Powell et al, 2004). Moreover, functional neuroimaging studies have shown that OFC and MTL are functionally connected during successful encoding (Ranganath, Heller, Cohen, Brozinsky, & Rissman, 2005), and are coactivated during the retrieval of positive autobiographical memories (Piefke, Weiss, Zilles, Markowitsch, & Fink, 2003). Yet, there is no direct evidence indicating that enhanced memory for happy faces reflects enhanced OFC and MTL activity and interactions between the two.…”

Section: Introductionmentioning

confidence: 99%

Orbitofrontal and hippocampal contributions to memory for face–name associations: The rewarding power of a smile

Tsukiura

Cabeza

2008

Neuropsychologia

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Memory processes can be enhanced by reward, and social signals such a smiling face can be rewarding to humans. Using event-related functional MRI (fMRI), we investigated the rewarding effect of a simple smile during the encoding and retrieval of face-name associations. During encoding, participants viewed smiling or neutral faces, each paired with a name, and during retrieval, only names were presented, and participants retrieved the associated facial expressions. Successful memory activity of face-name associations was identified by comparing remembered vs. forgotten trials during both encoding and retrieval, and the effect of a smile was identified by comparing successful memory trials for smiling vs. neutral faces. The study yielded three main findings. First, behavioral results showed that the retrieval of face-name associations was more accurate and faster for smiling than neutral faces. Second, the orbitofrontal cortex and the hippocampus showed successful encoding and retrieval activations, which were greater for smiling than neutral faces. Third, functional connectivity between the orbitofrontal cortex and the hippocampus during successful encoding and retrieval was stronger for smiling than neutral faces. As a part of reward system, the orbitofrontal cortex may modulate memory processes of face-name associations mediated by the hippocampus. Interestingly, the effect of a smile during retrieval was found even though only names were presented as retrieval cues, suggesting that the effect was mediated by face imagery. Taken together, the results demonstrate how rewarding social signals from a smiling face can enhance relational memory for face-name associations.

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“…For instance, the role of de novo protein synthesis and gene expression around training in both structures is critical for memory formation and consolidation (Bekinschtein et al 2007;Alberini 2009), which is in line with correlative studies in humans showing that successful memory formation is associated with an increase in functional connectivity between the hippocampus and some cortical regions, including RSC (Ranganath et al 2005). The timing of some molecular requirements, however, is different for each structure.…”

Section: [Supplemental Materials Is Available For This Article]supporting

confidence: 63%

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

Katche¹,

Dorman²,

Slipczuk

et al. 2013

Learn. Mem.

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Memory storage is a temporally graded process involving different phases and different structures in the mammalian brain. Cortical plasticity is essential to store stable memories, but little is known regarding its involvement in memory processing. Here we show that fear memory consolidation requires early post-training macromolecular synthesis in the anterior part of the retrosplenial cortex (aRSC), and that reversible pharmacological inactivation of this cortical region impairs recall of recent as well as of remote memories. These results challenge the generally accepted idea that neocortical areas are slow encoding systems that participate in the retrieval of remote memories only. [Supplemental material is available for this article.]A dominant idea that emerged in the last two decades is that memory consolidation comprises two phases. The initial one, called cellular or synaptic consolidation, is fast, lasting from several hours to a couple of days, and depends on de novo protein and mRNA synthesis required for functional and structural changes in brain regions engaged in the acquisition and early processing of new information, such as the hippocampus and related noncortical structures (Dudai 2002;Dudai and Eisenberg 2004;Morris 2006). The second phase is slower, and would entail the participation of neocortical regions and their interactions with medial temporal lobe structures reorganizing the recently learned material (Squire 1992). It is called systems-level consolidation and seems to begin late after acquisition and last from several days to weeks to months in most learning tasks studied so far (Frankland and Bontempi 2005). However, when recently encoded information interacts with an already stored associative schema, systems-level consolidation may well be very rapid (Tse et al. 2007(Tse et al. , 2011. Consistent with the standard model of memory consolidation, it has been shown that, while the hippocampus is mainly involved in consolidating and recalling recent episodic-like memories, some cortical regions, including prelimbic, orbitofrontal, and anterior cingulate areas, are involved preferentially with remote, well-consolidated memory traces (Frankland et al. 2004;Maviel et al. 2004;Shan et al. 2008;Lesburgueres et al. 2011;Tse et al. 2011).The retrosplenial cortex (RSC) comprises the entire posterior cingulate cortex in rodents (Vogt and Peters 1981) and is one of the largest cortical areas in the rat. Situated at the crossroads between the hippocampal formation and many neocortical areas, it has attracted much attention especially for its involvement in cognition (Vann et al. 2009). Although RSC inactivation produces memory impairments similar to those caused by hippocampal lesions (Cooper and Mizumori 2001;Vann and Aggleton 2004), and it has been shown that RSC is activated during retrieval of contextual information and autobiographical memory (Valenstein et al. 1987, Daselaar et al. 2006), the precise function of this area is poorly understood (Ranganath and Ritchey 2012).To study the precise r...

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Functional connectivity with the hippocampus during successful memory formation

Cited by 202 publications

References 77 publications

Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans

Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans

Orbitofrontal and hippocampal contributions to memory for face–name associations: The rewarding power of a smile

Functional integrity of the retrosplenial cortex is essential for rapid consolidation and recall of fear memory

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