Resolving New Memories: A Critical Look at the Dentate Gyrus, Adult Neurogenesis, and Pattern Separation

Aimone, James B.; Deng, Wei; Gage, Fred H.

doi:10.1016/j.neuron.2011.05.010

Cited by 574 publications

(500 citation statements)

References 49 publications

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“…In bilateral lateral PFC, and right parietal regions, responses to parametrically varied conceptual and perceptual input similarity provided further evidence for pattern separation. The data are in line with computational predictions (Treves and Rolls, 1992;Vazdarjanova and Guzowski, 2004) and with findings of pattern separation and completion computations in sensory cortex in rodents (Aimone et al, 2011;Barnes et al, 2008). Bilateral prefrontal and left occipital cortex regions showing pattern separation activity were also engaged during encoding predicting subsequent true recognition, consistent with suggestions that cortical pattern separation contributes to successful itemspecific encoding.…”

Section: Discussionsupporting

confidence: 88%

“…Our data suggest that pattern separation and pattern completion of perceptually and conceptually similar object representations extends beyond the hippocampus to prefrontal and occipito-temporal regions, supporting claims that these processes occur throughout the brain (Aimone et al, 2011;Barnes et al, 2008). By examining neural response to images varied in their similarity relative to previously viewed images, we provide evidence that the neural responses in several regions met computational predictions for pattern separation or completion for either or both perceptual and conceptual similarity.…”

Section: Discussionsupporting

confidence: 77%

“…Examining regions showing repetition suppression (Henson and Rugg, 2003), such investigations have reported activity consistent with pattern separation in a region spanning DG/CA3, and pattern completion activity in CA1 and elsewhere in the medial temporal lobe (MTL) (Bakker et al, 2008;Lacy et al, 2011). Although pattern separation and completion investigations have focussed on the role of the hippocampus, networks throughout the brain are thought to perform similar functions, including sensory cortex (Aimone et al, 2011;Gilbert and Kesner, 2003). Rodent electrophysiological recordings have demonstrated pattern separation of odour cues in the olfactory bulb, and pattern completion in piriform cortex (Barnes et al, 2008;Wilson, 2009), but these functions in regions outside the MTL have received little attention in studies in humans.…”

Section: Introductionmentioning

confidence: 99%

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Cortical pattern separation and item-specific memory encoding

Pidgeon

Morcom

2016

Neuropsychologia

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Pattern separation and pattern completion are fundamental brain processes thought to be critical for episodic memory encoding and retrieval, and for discrimination between similar memories. These processes are best understood in the hippocampus, but are proposed to occur throughout the brain, in particular in sensory regions. Cortical, as well as hippocampal, pattern separation may therefore support formation of event-unique memory traces. Using fMRI, we investigated cortical pattern separation and pattern completion and their relationship to encoding activity predicting subsequent item-specific compared to gist memory. During scanning, participants viewed images of novel objects, repeated objects, and objects which were both perceptually and conceptually similar to previously presented images, while performing a size judgement task. In a later surprise recognition test, they judged whether test items were 'same' 'similar' or 'new' relative to studied items. Activity consistent with pattern separation -responses to similar items as if novel -was observed in bilateral occipito-temporal cortex. Activity consistent with pattern completion -responses to similar items as if repeated -was observed in left prefrontal cortex and hippocampus. Curve fitting analysis further revealed that graded responses to change in image conceptual and perceptual similarity in bilateral prefrontal and right parietal regions met specific computational predictions for pattern separation for one or both of these similarity dimensions. Functional overlap between encoding activity predicting subsequent item-specific recognition and pattern separation activity was also observed in left occipital cortex and bilateral inferior frontal cortex. The findings suggest that extrahippocampal regions including sensory and prefrontal cortex contribute to pattern separation and pattern completion of visual input, consistent with the proposal that cortical pattern separation contributes to formation of item-specific memory traces, facilitating accurate recognition memory.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionsupporting

confidence: 77%

Section: Introductionmentioning

confidence: 99%

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Cortical pattern separation and item-specific memory encoding

Pidgeon

Morcom

2016

Neuropsychologia

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“…The DG is considered the “gatekeeper” of the trisynaptic glutamatergic throughput of the hippocampus (Tamminga, Southcott, Sacco, Wagner, & Ghose, 2012). The DG also has a high rate of neurogenesis (Aimone, Deng, & Gage, 2011). These factors may make the DG more susceptible to insults.…”

Section: Discussionmentioning

confidence: 99%

Linking kindling to increased glutamate release in the dentate gyrus of the hippocampus through the STXBP5/tomosyn‐1 gene

et al. 2017

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IntroductionIn kindling, repeated electrical stimulation of certain brain areas causes progressive and permanent intensification of epileptiform activity resulting in generalized seizures. We focused on the role(s) of glutamate and a negative regulator of glutamate release, STXBP5/tomosyn‐1, in kindling.MethodsStimulating electrodes were implanted in the amygdala and progression to two successive Racine stage 5 seizures was measured in wild‐type and STXBP5/tomosyn‐1−/− (Tom−/−) animals. Glutamate release measurements were performed in distinct brain regions using a glutamate‐selective microelectrode array (MEA).ResultsNaïve Tom−/− mice had significant increases in KCl‐evoked glutamate release compared to naïve wild type as measured by MEA of presynaptic release in the hippocampal dentate gyrus (DG). Kindling progression was considerably accelerated in Tom−/− mice, requiring fewer stimuli to reach a fully kindled state. Following full kindling, MEA measurements of both kindled Tom+/+ and Tom−/− mice showed significant increases in KCl‐evoked and spontaneous glutamate release in the DG, indicating a correlation with the fully kindled state independent of genotype. Resting glutamate levels in all hippocampal subregions were significantly lower in the kindled Tom−/− mice, suggesting possible changes in basal control of glutamate circuitry in the kindled Tom−/− mice.ConclusionsOur studies demonstrate that increased glutamate release in the hippocampal DG correlates with acceleration of the kindling process. Although STXBP5/tomosyn‐1 loss increased evoked glutamate release in naïve animals contributing to their prokindling phenotype, the kindling process can override any attenuating effect of STXBP5/tomosyn‐1. Loss of this “braking” effect of STXBP5/tomosyn‐1 on kindling progression may set in motion an alternative but ultimately equally ineffective compensatory response, detected here as reduced basal glutamate release.

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“…4 The rate at which new neurons are born depends on many factors, including exercise, stress, hormones, network activity; 5,6 and the DGCs that arise through adult neurogenesis are important in aspects of memory formation. 7,8 Disruption of either excitatory/ inhibitory balance or rates of adult neurogenesis causes neuropsychiatric disease: abnormal excitatory/inhibitory balance can lead to epilepsy, autism spectrum disorders, schizophrenia, cognitive processing, and anxiety disorders; 9,10,11,12 and abnormal neurogenesis is seen in depression, cognitive impairment, and epilepsy. 6,13 Together, these unique features of the hippocampal circuit demonstrate the importance of appropriate synapse development and maintenance of appropriate levels of neurogenesis into adulthood.…”

Section: Introductionmentioning

confidence: 99%