Learning-Facilitated Synaptic Plasticity at CA3 Mossy Fiber and Commissural-Associational Synapses Reveals Different Roles in Information Processing

Hagena, Hardy; Manahan‐Vaughan, Denise

doi:10.1093/cercor/bhq271

Cited by 78 publications

(131 citation statements)

References 44 publications

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“…3C). In concordance with PMT predictions, Manahan-Vaughn and coworkers have recently shown that directional cues facilitate long-term depression (LTD) in the dentate gyrus whereas positional cues facilitate LTD in CA1, and both cue types facilitate LTD in CA3 (27,28).…”

Section: Parallel Map Solutionmentioning

confidence: 65%

From chemotaxis to the cognitive map: The function of olfaction

Jacobs

2012

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

176

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A paradox of vertebrate brain evolution is the unexplained variability in the size of the olfactory bulb (OB), in contrast to other brain regions, which scale predictably with brain size. Such variability appears to be the result of selection for olfactory function, yet there is no obvious concordance that would predict the causal relationship between OB size and behavior. This discordance may derive from assuming the primary function of olfaction is odorant discrimination and acuity. If instead the primary function of olfaction is navigation, i.e., predicting odorant distributions in time and space, variability in absolute OB size could be ascribed and explained by variability in navigational demand. This olfactory spatial hypothesis offers a single functional explanation to account for patterns of olfactory system scaling in vertebrates, the primacy of olfaction in spatial navigation, even in visual specialists, and proposes an evolutionary scenario to account for the convergence in olfactory structure and function across protostomes and deuterostomes. In addition, the unique percepts of olfaction may organize odorant information in a parallel map structure. This could have served as a scaffold for the evolution of the parallel map structure of the mammalian hippocampus, and possibly the arthropod mushroom body, and offers an explanation for similar flexible spatial navigation strategies in arthropods and vertebrates.sensory | memory | orientation | limbic

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Section: Parallel Map Solutionmentioning

confidence: 65%

From chemotaxis to the cognitive map: The function of olfaction

Jacobs

2012

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

176

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“…Collectively, these studies highlight the importance of GPER1 and of the Akt/mTOR signaling pathway in estrogen modulation of learning and memory. In addition, mossy fiber LTD has been implicated in spatial memory (Hagena and Manahan-Vaughan, 2011), suggesting that the mechanism described here could play an important role in estrogen-induced cognitive enhancement. Because most behavioral studies with estrogen have been performed in ovariectomized rats, it would be important to study whether a similar modulation of mGluR-LTD by estrogen occurs in cycling females.…”

Section: Role Of the Ups In Mglur-ltdmentioning

confidence: 82%

A novel form of synaptic plasticity in field CA3 of hippocampus requires GPER1 activation and BDNF release

Briz¹,

Liu²,

Zhu³

et al. 2015

J Exp Med

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“…Exposure to a novel environment (e.g., empty holeboard) facilitates short-term potentiation (STP) into LTP (Kemp and Manahan-Vaughan, 2004, 2008; Hagena and Manahan-Vaughan, 2011). This phenomenon is observed when exploration coincides with high-frequency stimulation that is sub-threshold for LTP induction.…”

Section: Resultsmentioning

confidence: 99%

“…One the one hand, it shares properties with synapses of the dorsal hippocampus, where it was shown that exposure to novel space facilitates LTP (Manahan-Vaughan and Braunewell, 1999; Kemp and Manahan-Vaughan, 2008; Hagena and Manahan-Vaughan, 2011). On the other hand, in contrast to the dorsal hippocampus, where exposure to novel spatial contextual configurations facilitates persistent LTD (Manahan-Vaughan and Braunewell, 1999; Kemp and Manahan-Vaughan, 2004, 2008; Hagena and Manahan-Vaughan, 2011; Goh and Manahan-Vaughan, 2013), LTD in the intermediate dentate gyrus is not facilitated by this kind of novel spatial experience. Here, only STD was enhanced by novel landmark information, and somatic excitability (population spike amplitude) was transiently reduced by objects that were partially concealed in a holeboard.…”

Section: Discussionmentioning

confidence: 99%

“…The specific forms of facilitated synaptic plasticity depend on the particular hippocampal subregion, as well as on the nature of novel information presented to the animal. Exploration of a novel empty environment facilitates LTP in an input-specific manner at selected synapses in all main hippocampal subregions, whereas learning-dependent facilitation of LTD is subregion specific (Kemp and Manahan-Vaughan, 2004, 2008; Hagena and Manahan-Vaughan, 2011). Namely, in the dorsal dentate gyrus, exploration of large directional cues facilitates persistent LTD, whereas exposure to small, partially hidden cues has no effect on synaptic plasticity.…”

Section: Introductionmentioning

confidence: 99%

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Learning-facilitated synaptic plasticity occurs in the intermediate hippocampus in association with spatial learning

Kenney

Manahan‐Vaughan

2013

Front. Synaptic Neurosci.

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The dorsoventral axis of the hippocampus is differentiated into dorsal, intermediate, and ventral parts. Whereas the dorsal part is believed to specialize in processing spatial information, the ventral may be equipped to process non-spatial information. The precise role of the intermediate hippocampus is unclear, although recent data suggests it is functionally distinct, at least from the dorsal hippocampus. Learning-facilitated synaptic plasticity describes the ability of hippocampal synapses to respond with robust synaptic plasticity (>24 h) when a spatial learning event is coupled with afferent stimulation that would normally not lead to a lasting plasticity response: in the dorsal hippocampus novel space facilitates robust expression of long-term potentiation (LTP), whereas novel spatial content facilitates long-term depression (LTD). We explored whether the intermediate hippocampus engages in this kind of synaptic plasticity in response to novel spatial experience. In freely moving rats, high-frequency stimulation at 200 Hz (3 bursts of 15 stimuli) elicited synaptic potentiation that lasted for at least 4 h. Coupling of this stimulation with the exploration of a novel holeboard resulted in LTP that lasted for over 24 h. Low frequency afferent stimulation (1 Hz, 900 pulses) resulted in short-term depression (STD) that was significantly enhanced and prolonged by exposure to a novel large orientational (landmark) cues, however LTD was not enabled. Exposure to a holeboard that included novel objects in the holeboard holes elicited a transient enhancement of STD of the population spike (PS) but not field EPSP, and also failed to facilitate the expression of LTD. Our data suggest that the intermediate dentate gyrus engages in processing of spatial information, but is functionally distinct to the dorsal dentate gyrus. This may in turn reflect their assumed different roles in synaptic information processing and memory formation.

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Learning-Facilitated Synaptic Plasticity at CA3 Mossy Fiber and Commissural-Associational Synapses Reveals Different Roles in Information Processing

Cited by 78 publications

References 44 publications

From chemotaxis to the cognitive map: The function of olfaction

From chemotaxis to the cognitive map: The function of olfaction

A novel form of synaptic plasticity in field CA3 of hippocampus requires GPER1 activation and BDNF release

Learning-facilitated synaptic plasticity occurs in the intermediate hippocampus in association with spatial learning

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