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Article ; Online: The hippocampus contributes to retroactive stimulus associations during trace fear conditioning.

Puhger, Kyle / Crestani, Ana P / Diniz, Cassiano R A F / Wiltgen, Brian J

iScience

2024 Volume 27, Issue 3, Page(s) 109035

Abstract: Binding events that occur at different times are essential for memory formation. In trace fear conditioning, animals associate a tone and footshock despite no temporal overlap. The hippocampus is thought to mediate this learning by maintaining a memory ... ...

Abstract	Binding events that occur at different times are essential for memory formation. In trace fear conditioning, animals associate a tone and footshock despite no temporal overlap. The hippocampus is thought to mediate this learning by maintaining a memory of the tone until shock occurrence, however, evidence for sustained hippocampal tone representations is lacking. Here, we demonstrate a retrospective role for the hippocampus in trace fear conditioning. Bulk calcium imaging revealed sustained increases in CA1 activity after footshock that were not observed after tone termination. Optogenetic silencing of CA1 immediately after footshock impaired subsequent memory. Additionally, footshock increased the number of sharp-wave ripples compared to baseline during conditioning. Therefore, post-shock hippocampal activity likely supports learning by reactivating and linking latent tone and shock representations. These findings highlight an underappreciated function of post-trial hippocampal activity in enabling retroactive temporal associations during new learning, as opposed to persistent maintenance of stimulus representations.
Language	English
Publishing date	2024-01-26
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2024.109035
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Article ; Online: Phasic locus coeruleus activity enhances trace fear conditioning by increasing dopamine release in the hippocampus.

Wilmot, Jacob H / Diniz, Cassiano R A F / Crestani, Ana P / Puhger, Kyle R / Roshgadol, Jacob / Tian, Lin / Wiltgen, Brian Joseph

eLife

2024 Volume 12

Abstract: Locus coeruleus (LC) projections to the hippocampus play a critical role in learning and memory. However, the precise timing of LC-hippocampus communication during learning and which LC-derived neurotransmitters are important for memory formation in the ... ...

Abstract	Locus coeruleus (LC) projections to the hippocampus play a critical role in learning and memory. However, the precise timing of LC-hippocampus communication during learning and which LC-derived neurotransmitters are important for memory formation in the hippocampus are currently unknown. Although the LC is typically thought to modulate neural activity via the release of norepinephrine, several recent studies have suggested that it may also release dopamine into the hippocampus and other cortical regions. In some cases, it appears that dopamine release from LC into the hippocampus may be more important for memory than norepinephrine. Here, we extend these data by characterizing the phasic responses of the LC and its projections to the dorsal hippocampus during trace fear conditioning in mice. We find that the LC and its projections to the hippocampus respond to task-relevant stimuli and that amplifying these responses with optogenetic stimulation can enhance long-term memory formation. We also demonstrate that LC activity increases both norepinephrine and dopamine content in the dorsal hippocampus and that the timing of hippocampal dopamine release during trace fear conditioning is similar to the timing of LC activity. Finally, we show that hippocampal dopamine is important for trace fear memory formation, while norepinephrine is not.
MeSH term(s)	Animals ; Mice ; Dopamine ; Locus Coeruleus ; Fear ; Hippocampus ; Norepinephrine
Chemical Substances	Dopamine (VTD58H1Z2X) ; Norepinephrine (X4W3ENH1CV)
Language	English
Publishing date	2024-04-09
Publishing country	England
Document type	Journal Article
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.91465
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Article: Acute Disruption of the Dorsal Hippocampus Impairs the Encoding and Retrieval of Trace Fear Memories.

Wilmot, Jacob H / Puhger, Kyle / Wiltgen, Brian J

Frontiers in behavioral neuroscience

2019 Volume 13, Page(s) 116

Abstract: A major function of the hippocampus is to link discontiguous events in memory. This process can be studied in animals using Pavlovian trace conditioning, a procedure where the conditional stimulus (CS) and unconditional stimulus (US) are separated in ... ...

Abstract	A major function of the hippocampus is to link discontiguous events in memory. This process can be studied in animals using Pavlovian trace conditioning, a procedure where the conditional stimulus (CS) and unconditional stimulus (US) are separated in time. While the majority of studies have found that trace conditioning requires the dorsal segment of the hippocampus, others have not. This variability could be due to the use of lesion and pharmacological techniques, which lack cell specificity and temporal precision. More recent studies using optogenetic tools find that trace fear acquisition is disrupted by decreases in dorsal CA1 (dCA1) activity while increases lead to learning enhancements. However, comparing these results is difficult given that some studies manipulated the activity of CA1 pyramidal neurons directly and others did so indirectly (e.g.,
Language	English
Publishing date	2019-05-29
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2019.00116
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Article ; Online: Reply to 'Active and effective replay: systems consolidation reconsidered again'.

Yonelinas, Andrew P / Ranganath, Charan / Ekstrom, Arne D / Wiltgen, Brian J

Nature reviews. Neuroscience

2019 Volume 20, Issue 8, Page(s) 507–508

MeSH term(s)	Memory, Episodic
Language	English
Publishing date	2019-06-03
Publishing country	England
Document type	Letter ; Comment
ZDB-ID	2034150-7
ISSN	1471-0048 ; 1471-0048 ; 1471-003X
ISSN (online)	1471-0048
ISSN	1471-0048 ; 1471-003X
DOI	10.1038/s41583-019-0192-7
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Zs.A 5473: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: A contextual binding theory of episodic memory: systems consolidation reconsidered.

Yonelinas, Andrew P / Ranganath, Charan / Ekstrom, Arne D / Wiltgen, Brian J

Nature reviews. Neuroscience

2019 Volume 20, Issue 6, Page(s) 364–375

Abstract: Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as ... ...

Abstract	Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as sleep to neocortical areas for long-term storage. Here, we propose an alternative to this standard systems consolidation theory (SSCT) - a contextual binding account - in which the hippocampus binds item-related and context-related information. We compare these accounts in light of behavioural, lesion, neuroimaging and sleep studies of episodic memory and contend that forgetting is largely due to contextual interference, episodic memory remains dependent on the hippocampus across time, contextual drift produces post-encoding activity and sleep benefits memory by reducing contextual interference.
MeSH term(s)	Animals ; Hippocampus/physiology ; Humans ; Memory, Episodic ; Mental Recall/physiology ; Sleep/physiology
Language	English
Publishing date	2019-03-15
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2034150-7
ISSN	1471-0048 ; 1471-0048 ; 1471-003X
ISSN (online)	1471-0048
ISSN	1471-0048 ; 1471-003X
DOI	10.1038/s41583-019-0150-4
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Article ; Online: Systems consolidation and the content of memory.

Wiltgen, Brian J / Tanaka, Kazumasa Z

Neurobiology of learning and memory

2013 Volume 106, Page(s) 365–371

Abstract: Systems consolidation is the process by which memories become independent of the hippocampus and stored in regions of the neocortex. This process is commonly studied in rodents using context fear conditioning. It is becoming increasingly clear, however, ... ...

Abstract	Systems consolidation is the process by which memories become independent of the hippocampus and stored in regions of the neocortex. This process is commonly studied in rodents using context fear conditioning. It is becoming increasingly clear, however, that context memories do not always undergo systems consolidation. To explain this fact, the current review describes a number of factors that determine whether or not context fear can be retrieved without the hippocampus during remote memory tests. These include neurogenesis, the presentation of reminder cues after learning, the quality of the memory that is retrieved during testing and the method that is used to inactivate the hippocampus. Based on these data, we propose that remote context fear memories can be retrieved by either the hippocampus or the neocortex. Tests of memory quality (e.g. context discrimination) can typically be used to determine which system is engaged during retrieval. The same is not true of recently formed context fear memories, which appear to always require the hippocampus during retrieval.
MeSH term(s)	Animals ; Conditioning (Psychology)/physiology ; Fear/physiology ; Hippocampus/physiology ; Memory/physiology ; Memory, Long-Term/physiology ; Mental Recall/physiology ; Neocortex/physiology
Language	English
Publishing date	2013-11
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1223366-3
ISSN	1095-9564 ; 1074-7427
ISSN (online)	1095-9564
ISSN	1074-7427
DOI	10.1016/j.nlm.2013.06.001
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Article ; Online: New methods for understanding systems consolidation.

Tayler, Kaycie K / Wiltgen, Brian J

Learning & memory (Cold Spring Harbor, N.Y.)

2013 Volume 20, Issue 10, Page(s) 553–557

Abstract: According to the standard model of systems consolidation (SMC), neocortical circuits are reactivated during the retrieval of declarative memories. This process initially requires the hippocampus. However, with the passage of time, neocortical circuits ... ...

Abstract	According to the standard model of systems consolidation (SMC), neocortical circuits are reactivated during the retrieval of declarative memories. This process initially requires the hippocampus. However, with the passage of time, neocortical circuits become strengthened and can eventually retrieve memory without input from the hippocampus. Although consistent with lesion data, these assumptions have been difficult to confirm experimentally. In the current review, we discuss recent methodological advances in behavioral neuroscience that are making it possible to test the basic assumptions of SMC for the first time. For example, new transgenic mice can be used to monitor the activity of individual neurons across the entire brain while optogenetic approaches provide precise control over the activity of these cells using light stimulation. These tools can be used to examine the reactivation of neocortical neurons during recent and remote memory retrieval and determine if this process requires the hippocampus.
MeSH term(s)	Animals ; Humans ; Memory/physiology ; Mice, Transgenic ; Neocortex/physiology ; Neurons/physiology ; Neurosciences/methods ; Neurosciences/trends
Language	English
Publishing date	2013-09-16
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	1204777-6
ISSN	1549-5485 ; 1072-0502
ISSN (online)	1549-5485
ISSN	1072-0502
DOI	10.1101/lm.029454.112
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Zs.A 4107: Show issues

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Article ; Online: Memory retrieval along the proximodistal axis of CA1.

Nakazawa, Yuki / Pevzner, Aleksandr / Tanaka, Kazumasa Z / Wiltgen, Brian J

Hippocampus

2016 Volume 26, Issue 9, Page(s) 1140–1148

Abstract: The proximal and distal segments of CA1 are thought to perform distinct computations. Neurons in proximal CA1 are reciprocally connected with the medial entorhinal cortex (MEC) and exhibit precise spatial firing. In contrast, cells in distal CA1 ... ...

Abstract	The proximal and distal segments of CA1 are thought to perform distinct computations. Neurons in proximal CA1 are reciprocally connected with the medial entorhinal cortex (MEC) and exhibit precise spatial firing. In contrast, cells in distal CA1 communicate with the lateral entorhinal cortex (LEC), exhibit more diffuse spatial firing and are affected by the presence of objects in the environment. To determine if these segments make unique contributions to memory retrieval, we examined cellular activity along the proximodistal axis of CA1 using transgenic reporter mice. Neurons tagged during context learning in proximal CA1 were more likely to be reactivated during testing than those in distal CA1. This was true following context fear conditioning and after exposure to a novel environment. Reactivation was also higher in brain regions connected to proximal CA1 (MEC, distal CA3) than those connected to the distal segment (LEC, proximal CA3). To examine contributions to memory retrieval, we performed neurotoxic lesions of proximal or distal CA1 after training. Lesions of the proximal segment significantly impaired memory retrieval while damage to distal CA1 had no effect. These data suggest that context memories are retrieved by a hippocampal microcircuit that involves the proximal but not distal segment of CA1. © 2016 Wiley Periodicals, Inc.
Language	English
Publishing date	2016-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	1074352-2
ISSN	1098-1063 ; 1050-9631
ISSN (online)	1098-1063
ISSN	1050-9631
DOI	10.1002/hipo.22596
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Article: High-Frequency Stimulation of Ventral CA1 Neurons Reduces Amygdala Activity and Inhibits Fear.

Graham, Jalina / D'Ambra, Alexa F / Jung, Se Jung / Teratani-Ota, Yusuke / Vishwakarma, Nina / Venkatesh, Rasika / Parigi, Abhijna / Antzoulatos, Evan G / Fioravante, Diasynou / Wiltgen, Brian J

Frontiers in behavioral neuroscience

2021 Volume 15, Page(s) 595049

Abstract: The hippocampus can be divided into distinct segments that make unique contributions to learning and memory. The dorsal segment supports cognitive processes like spatial learning and navigation while the ventral hippocampus regulates emotional behaviors ... ...

Abstract	The hippocampus can be divided into distinct segments that make unique contributions to learning and memory. The dorsal segment supports cognitive processes like spatial learning and navigation while the ventral hippocampus regulates emotional behaviors related to fear, anxiety and reward. In the current study, we determined how pyramidal cells in ventral CA1 respond to spatial cues and aversive stimulation during a context fear conditioning task. We also examined the effects of high and low frequency stimulation of these neurons on defensive behavior. Similar to previous work in the dorsal hippocampus, we found that cells in ventral CA1 expressed high-levels of c-Fos in response to a novel spatial environment. Surprisingly, however, the number of activated neurons did not increase when the environment was paired with footshock. This was true even in the subpopulation of ventral CA1 pyramidal cells that send direct projections to the amygdala. When these cells were stimulated at high-frequencies (20 Hz) we observed feedforward inhibition of basal amygdala neurons and impaired expression of context fear. In contrast, low-frequency stimulation (4 Hz) did not inhibit principal cells in the basal amygdala and produced an increase in fear generalization. Similar results have been reported in dorsal CA1. Therefore, despite clear differences between the dorsal and ventral hippocampus, CA1 neurons in each segment appear to make similar contributions to context fear conditioning.
Language	English
Publishing date	2021-03-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452960-6
ISSN	1662-5153
ISSN	1662-5153
DOI	10.3389/fnbeh.2021.595049
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Article ; Online: Metaplasticity contributes to memory formation in the hippocampus.

Crestani, Ana P / Krueger, Jamie N / Barragan, Eden V / Nakazawa, Yuki / Nemes, Sonya E / Quillfeldt, Jorge A / Gray, John A / Wiltgen, Brian J

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2018 Volume 44, Issue 2, Page(s) 408–414

Abstract: Prior learning can modify the plasticity mechanisms that are used to encode new information. For example, NMDA receptor (NMDAR) activation is typically required for new spatial and contextual learning in the hippocampus. However, once animals have ... ...

Abstract	Prior learning can modify the plasticity mechanisms that are used to encode new information. For example, NMDA receptor (NMDAR) activation is typically required for new spatial and contextual learning in the hippocampus. However, once animals have acquired this information, they can learn new tasks even if NMDARs are blocked. This finding suggests that behavioral training alters cellular plasticity mechanisms such that NMDARs are not required for subsequent learning. The mechanisms that mediate this change are currently unknown. To address this issue, we tested the idea that changes in intrinsic excitability (induced by learning) facilitate the encoding of new memories via metabotropic glutamate receptor (mGluR) activation. Consistent with this hypothesis, hippocampal neurons exhibited increases in intrinsic excitability after learning that lasted for several days. This increase was selective and only observed in neurons that were activated by the learning event. When animals were trained on a new task during this period, excitable neurons were reactivated and memory formation required the activation of mGluRs instead of NMDARs. These data suggest that increases in intrinsic excitability may serve as a metaplastic mechanism for memory formation.
MeSH term(s)	Animals ; Conditioning, Classical/drug effects ; Excitatory Amino Acid Antagonists/pharmacology ; Hippocampus/drug effects ; Male ; Memory/drug effects ; Mice ; Neuronal Plasticity/drug effects ; Neurons/drug effects ; Patch-Clamp Techniques ; Receptors, Metabotropic Glutamate/antagonists & inhibitors ; Receptors, N-Methyl-D-Aspartate/antagonists & inhibitors ; Valine/analogs & derivatives ; Valine/pharmacology
Chemical Substances	Excitatory Amino Acid Antagonists ; Receptors, Metabotropic Glutamate ; Receptors, N-Methyl-D-Aspartate ; 2-amino-5-phosphopentanoic acid (76326-31-3) ; Valine (HG18B9YRS7)
Language	English
Publishing date	2018-05-16
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/s41386-018-0096-7
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