Making context memories independent of the hippocampus

Lehmann, Hugo; Sparks, Fraser T.; Spanswick, Simon C.; Hadikin, Crystal; McDonald, Robert J.; Sutherland, Robert J.

doi:10.1101/lm.1385409

Cited by 71 publications

(74 citation statements)

References 35 publications

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“…A common feature of these studies is that the rodents only received a single fear-conditioning session, often with multiple shock presentations within the session. Recently, Lehmann et al (2009) replicated the results obtained with a single sessionsevere retrograde amnesia. However, they also reported that if these …”

Section: Contextual Fear Conditioningsupporting

confidence: 77%

“…In fact, if only the anterograde data were available, there would be little reason to believe that the hippocampal formation is involved in contextual fear conditioning. However, studies using a retrograde procedure reveal a different outcome-damage to the hippocampal formation after conditioning can almost completely eliminate contextual fear conditioning (Maren et al 1997;Maren 1999;Wiltgen et al 2006;Lehmann et al 2007Lehmann et al , 2009Sutherland et al 2008;Biedenkapp and Rudy 2009).…”

Section: Contextual Fear Conditioningmentioning

confidence: 99%

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Context representations, context functions, and the parahippocampal–hippocampal system

Rudy¹

2009

Learn. Mem.

266

309

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Psychologists and neurobiologists have a long-standing interest in understanding how the context surrounding the events of our lives is represented and how it influences our behavior. The hippocampal formation emerged very early as a major contributor to how context is represented and functions. There is a large literature examining its contribution that on the surface reveals an array of conflicting outcomes and controversy. This review reveals that these conflicts can be resolved by building Nadel and Willner's dual-process theory of context representations. Two general conclusions emerge: (1) There are two neural systems that can support context representations and functions-a neocortical system composed primarily of perirhinal and postrhinal cortices and a hippocampal system that includes perirhinal, postrhinal, entorhinal cortices, and the hippocampal formation. (2) These two systems are not equivalent-some context representations and functions are uniquely supported by the hippocampal system. These conclusions are discussed in the context of canonical ideas about the special properties of the hippocampal system that enable it to make unique contributions to memory.Everything we experience happens somewhere. The term ''context'' is often used to denote this ''somewhere.'' In the analysis of learning and memory, the context is like the setting for a stage play (Medin and Reynolds 1985). It provides the background for the real action in the drama-the main events. More importantly, as a consequence of learning and memory processes, the context often helps to select appropriate behaviors and determine the explicit and implicit content of our thoughts. Thus, it is not surprising that psychologists have a long-standing empirical and theoretical interest in understanding just what makes up a representation of context and how context representations interact with the main events of our lives to influence our behavior (see Balsam and Tomie 1985).More recently, neurobiologists have increased their interest in the problem of linking context representations and functions to brain systems. The hippocampal formation emerged quite early as a major focal point among many researchers. As a result, there is a substantial literature linking the hippocampal formation and context. However, on the surface, this research yields a dismaying set of conflicting results, with many findings that the hippocampal formation plays a critical role in supporting the influence of context on memory and behavior and many other findings that it does not.The goal of this article is to bring some clarity and order to this state of affairs. I start by providing a working definition of ''context'' that implicitly underpins its experimental analysis. I then describe several different functions of context that have been studied in the laboratory and are assumed to be theoretically important. I then introduce and build on a dual-process theory of context representations that was put forth several years ago by Lynn Nadel, Jeffrey Willner, and colleague...

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Section: Contextual Fear Conditioningsupporting

confidence: 77%

Section: Contextual Fear Conditioningmentioning

confidence: 99%

Context representations, context functions, and the parahippocampal–hippocampal system

Rudy¹

2009

Learn. Mem.

266

309

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“…They argued that the maintenance of episodic memories requires hippocampal activity indefinitely, but that repeated training could support recall independent of the hippocampus by facilitating acquisition by extra-hippocampal circuits which nominally participate in a task, but are overshadowed by hippocampal activity. This effect has been noted following repeated training in contextual fear conditioning (Lehmann et al, 2009) and spatial navigation (Winocur et al, 2005).…”

Section: Histologymentioning

confidence: 83%

“…There are other factors not addressed by the present study that may also contribute to systems consolidation. For instance, training that occurs over multiple distributed sessions can mitigate the necessity of the hippocampus for recall (Lehmann et al, 2009;Winocur et al, 2005). This idea was first suggested by Nadel and Moscovitch (1997) in their description of the Multiple Trace Theory of hippocampal-dependent systems consolidation.…”

Section: Histologymentioning

confidence: 99%

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Cox

Czerniawski

Ree

et al. 2013

Neurobiology of Learning and Memory

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It is becoming increasingly clear that the time-dependent involvement of the hippocampus in the recall of acquired behaviors is more complicated than once thought.Several early studies demonstrated that hippocampal damage attenuates the expression of recent, but not remotely trained tasks. By contrast, an emerging body of evidence has shown that damage to, or inactivation of, the hippocampus impairs recall across a wide range of training-testing intervals. Collectively, these data suggest that the time course of hippocampal involvement in the storage or recall of previouslyacquired memories differs according to hippocampal subregion and the particular learning task under consideration. The present study examined the contributions of dorsal (DH) and ventral (VH) hippocampus to the expression of previously-acquired trace fear conditioning, a form of Pavlovian conditioning in which the presentation of an initially neutral cue or cues and a subsequent aversive stimulus is separated by a nostimulus (trace) interval. Specifically, either the GABA-A agonist muscimol or saline was ii infused into the DH or VH prior to testing 1, 7, 28, or 42 days after trace fear conditioning. The results revealed a marked dissociation: pre-testing inactivation of DH failed to impair performance at any time-point, while pre-testing inactivation of VH impaired performance at all time-points. Importantly, pre-testing inactivation of VH had no effect on the performance during testing of previously-acquired delay conditioning.Collectively, these data suggest that VH, but not DH, remains a neuroanatomical locus critical to the recall or expression of trace fear conditioning over an extended period of time.

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“…These findings add to a body of evidence that the hippocampus is necessary when contextual information is important. We also confirm that memory deficits after chronic adrenalectomy are not a result of loss of corticosterone per se.Research with rats (Sutherland and McDonald 1990;Kim and Faneslow 1992;Anagnostaras et al 2001;Lehmann et al 2009), nonhuman primates (Machado and Bachevalier 2006;Pascalis et al 2009), and humans (Alvarez et al 2008;Marschner et al 2008) shows that hippocampal damage can disrupt the ability to recall or express information about context. Furthermore, several reports suggest that the hippocampus is important for creating flexible representations of context and object associations.…”

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confidence: 99%

Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

Spanswick¹,

Sutherland²

2010

Learn. Mem.

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Chronic adrenalectomy (ADX) causes a gradual and selective loss of granule cells in the dentate gyrus (DG) of the rat. Here, we administered replacement corticosterone to rats beginning 10 wk after ADX. We then tested them in three discrimination tasks based on object novelty, location, or object/context association. Only during testing of the object/context association did ADX rats demonstrate deficits. These findings add to a body of evidence that the hippocampus is necessary when contextual information is important. We also confirm that memory deficits after chronic adrenalectomy are not a result of loss of corticosterone per se.Research with rats (Sutherland and McDonald 1990;Kim and Faneslow 1992;Anagnostaras et al. 2001;Lehmann et al. 2009), nonhuman primates (Machado and Bachevalier 2006;Pascalis et al. 2009), and humans (Alvarez et al. 2008;Marschner et al. 2008) shows that hippocampal damage can disrupt the ability to recall or express information about context. Furthermore, several reports suggest that the hippocampus is important for creating flexible representations of context and object associations. Studies in rats (Mumby et al. 2002;O'Brien et al. 2006) and humans (Pascalis et al. 2009) show that lesions specific to the hippocampus produce deficits in object recognition only when contextual information is altered.Within the hippocampus, the dentate gyrus (DG) is important for certain aspects of memory (Xavier et al. 1999;Garthe et al. 2009). Chronic adrenalectomy (ADX) causes a gradual and selective loss of granule cells in the DG of the rat (Sloviter et al. 1989). This loss of cells is attributed to a lack of circulating corticosterone (CORT) (Sloviter et al. 1989;Woolley et al. 1991). Behavioral deficits as a result of chronic ADX have been reported in the Morris water task (Armstrong et al. 1993;Roozendaal et al. 1998;Spanswick et al. 2007) and open-field task (Islam et al. 1995). There has been debate as to whether the deficits experienced by ADX rats are a result of lost CORT or due to the depletion of the granule cell layer itself. Conrad and Roy (1995) and McCormick et al. (1997) report that acute CORT replacement is sufficient to alleviate some of the deficits in spatial tasks associated with chronic ADX. These findings have led some to conclude that the removal of CORT is responsible for the behavioral deficits experienced by ADX rats and not the loss of granule cells per se. In direct contrast to these findings, Spanswick et al. (2007) report that administration of CORT after 6 wk of ADX does not alleviate spatial deficits in a moving-platform version of the Morris water task. Also in opposition to Conrad and Roy (1995) and McCormick et al. (1997), studies utilizing colchicine as a method to remove granule cells report spatial deficits as a result of cell loss (Sutherland et al. 1983;Xavier et al. 1999;Jeltsch et al. 2001).Here, we show using three versions of a novelty-preference task (novel object, novel place, and object/context mismatch) that lesions limited to the granule cell layer...

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Making context memories independent of the hippocampus

Cited by 71 publications

References 35 publications

Context representations, context functions, and the parahippocampal–hippocampal system

Context representations, context functions, and the parahippocampal–hippocampal system

Time course of dorsal and ventral hippocampal involvement in the expression of trace fear conditioning

Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

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