Functional cross‐hemispheric shift between object‐place paired associate memory and spatial memory in the human hippocampus

Lee, Choong-Hee; Ryu, Jiho; Lee, Sang-Hun; Kim, Hak-Jin; Lee, Inah

doi:10.1002/hipo.22587

Cited by 21 publications

(20 citation statements)

References 56 publications

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“…The role of the left side has been suggested to relate to the transfer of recently formed memories to long-term storage (in rats, [22]) or function in autobiographical memory formation (in humans, [30]). More recently, the left hippocampal formation in humans has been shown to be preferentially active during an object recognition task [3,4] whereas the right hippocampus showed greater response in a place task [4]. It is intriguing that we found similar left side preference for object processing in mice, suggesting perhaps greater functional parallels between humans and rodents than has been recognized.…”

Section: Discussionsupporting

confidence: 51%

“…In humans, both hippocampal hemispheres are recruited during spatial navigation, although activity in only the right hippocampus corresponds to navigation accuracy [2]. Conversely, the left entorhinal cortex appears to be specialized for object encoding [3] and the left hippocampus is specialized for object-cued spatial memory [4]. Spatial navigation involves actual or imagined self-motion through a real or virtual environment, whereas object memory consists of the processing of externally originating sensory stimuli; invoking a long-held dichotomy in the characteristics of information integrated by the hippocampus described in the cognitive map theory [5].…”

Section: Introductionmentioning

confidence: 99%

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Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

2019

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Hemispheric lateralization is a fundamental organizing principle of nervous systems across taxonomic groups with bilateral symmetry. The mammalian hippocampus is lateralized anatomically, physiologically, and chemically; however, functional asymmetries are not yet well understood. Imaging studies in humans have implicated the left and right hippocampus in specialized processing. However, it is not clear if lateralized activity occurs in the rodent hippocampus. c-Fos imaging in animals provides a measure of neuronal activity with a resolution at the level of single cells. The aim of the present study was to determine whether lateralized activity-dependent c-Fos expression occurs in the rodent hippocampus. To understand functional lateralization of hippocampal processing, we compared interhemispheric expression of c-Fos in the dentate gyrus (DG), a structure involved in encoding new experiences, in mice that ran on a wheel, encoded a novel object, or remained in home cages. We found that wheel running (WR) induced the greatest amount of DG c-Fos expression in both hemispheres, with no difference between hemispheres. Object exploration (OB) resulted in left-lateralized DG c-Fos expression, whereas control (CON) mice were not lateralized. We then sought to determine whether differential consideration of hemispheres might influence the conclusions of a study by simulating common cell quantitation methods. We found that different approaches led to different conclusions. These data demonstrate lateralization of neuronal activity in the mouse DG corresponding to the experience of the animal and show that differentially considering hemisphere leads to alternative conclusions.

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Section: Discussionsupporting

confidence: 51%

Section: Introductionmentioning

confidence: 99%

Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

2019

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“…Animals and Housing. Adult male (n=23) and female (n=22) C57Bl6 mice (Jackson Labs) were group housed (3)(4) in standard shoebox plastic caging with bedding on a 12 hr light/dark cycle with free access to food and water. Behavior.…”

Section: Methods and Experimental Designmentioning

confidence: 99%

Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Jordan

Pytte

2017

Preprint

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Hemispheric lateralization is a fundamental organizing principle of nervous systems across taxonomic groups with bilateral symmetry. The mammalian hippocampus is lateralized anatomically, physiologically, and chemically; however, functional asymmetries are not yet well understood. Imaging studies in humans have implicated the left and right hippocampus in specialized processing. However, it is not clear if lateralized activity occurs in the rodent hippocampus. c-Fos imaging in animals provides a measure of neuronal activity with a resolution at the level of single cells. The aim of this study was to determine whether lateralized activity-dependent c-Fos expression occurs in the rodent hippocampus. To understand functional lateralization of hippocampal processing, we compared interhemispheric expression of c-Fos in the dentate gyrus (DG), a structure involved in encoding new experiences, in mice that ran on a wheel, encoded a novel object, or remained in home cages. We found that wheel running induced the greatest amount of DG c-Fos expression in both hemispheres, with no difference between hemispheres. Object exploration resulted in left-lateralized DG c-Fos expression, whereas control mice were not lateralized. We then sought to determine whether differential consideration of hemispheres might influence the conclusions of a study by simulating common cell quantification methods. We found that different approaches led to different conclusions. These data demonstrate lateralization of neuronal activity in the mouse DG corresponding to the experience of the animal and show that differentially considering hemisphere leads to alternative conclusions.

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“…We then grand-averaged the P1w peak amplitude for EC and FG stimulation separately in each individual patient, when the stimulation is delivered to more than one electrode pair in each region. Recently, Lee, Ryu, Lee, Kim, and Lee (2016) showed in human fMRI study that the efficient retrieval of object-place paired associate memory was correlated with the BOLD response of the left hippocampus, whereas the efficient retrieval of relatively pure spatial memory was correlated with the right hippocampal BOLD response, suggesting that the left and right hippocampus process qualitatively different information for remembering episodic events in space. Thus, we expect that both the left and right hippocampus may have an important role in episodic memory function.…”

Section: Correlation Between P1w Peak Amplitude and Neuropsychologimentioning

confidence: 99%

Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings

et al. 2019

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Objective We aimed at clarifying the clinical significance of the responses evoked by human entorhinal cortex (EC) electrical stimulation by means of cortico‐cortical evoked potentials (CCEPs). Methods We enrolled nine patients with medically intractable medial temporal lobe epilepsy who underwent invasive presurgical evaluations with subdural or depth electrodes. Single‐pulse electrical stimulation was delivered to the EC and fusiform gyrus (FG), and their evoked potentials were compared. The correlation between the evoked potentials and Wechsler Memory Scale‐Revised (WMS‐R) score was analyzed to investigate whether memory circuit was involved in the generation of the evoked potentials. Results In most electrodes placed on the neocortex, EC stimulation induced unique evoked potentials with positive polarity, termed as “widespread P1” (P1w). Compared with FG stimulation, P1w induced by EC stimulation were distinguished by their high occurrence rate, short peak latency (mean: 20.1 ms), small peak amplitude, and waveform uniformity among different recording sites. A stimulation of more posterior parts of the EC induced P1w with shorter latency and larger amplitude. P1w peak amplitude had a positive correlation (r = .69) with the visual memory score of the WMS‐R. In one patient, with depth electrode implanted into the hippocampus, the giant evoked potentials were recorded in the electrodes of the anterior hippocampus and EC near the stimulus site. Conclusions The human EC electrical stimulation evoked the short‐latency potentials in the broad neocortical regions. The origin of P1w remains unclear, although the limited evidence suggests that P1w is the far‐field potential by the volume conduction of giant evoked potential from the EC itself and hippocampus. The significance of the present study is that those evoked potentials may be a potential biomarker of memory impairment in various neurological diseases, and we provided direct evidence for the functional subdivisions along the anterior–posterior axis in the human EC.

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Functional cross‐hemispheric shift between object‐place paired associate memory and spatial memory in the human hippocampus

Cited by 21 publications

References 56 publications

Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Behavioral state-dependent lateralization of dorsal dentate gyrus c-Fos expression in mice

Human entorhinal cortex electrical stimulation evoked short‐latency potentials in the broad neocortical regions: Evidence from cortico‐cortical evoked potential recordings

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