Right‐hemispheric dominance of spatial memory in split‐brain mice

Shinohara, Yuta; Hosoya, Aki; Yamasaki, Nobuyuki; Ahmed, Hassan; Hattori, Satoko; Eguchi, Megumi; Yamaguchi, Shun; Miyakawa, Tsuyoshi; Hirase, Hajime; Shigemoto, Ryuichi

doi:10.1002/hipo.20886

Cited by 65 publications

(62 citation statements)

References 15 publications

(17 reference statements)

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“…These results support findings that both hippocampal hemispheres contribute to spatial learning [30]. MWM Fixed Platform acquisition deficits [5,11] have been shown in right hemisphere injury, though contrary to the present findings, others have noted acquisition deficits also from left lateral injuries [9,10].…”

Section: Discussionsupporting

confidence: 84%

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Investigation of left and right lateral fluid percussion injury in C57BL6/J mice: In vivo functional consequences

Schurman

Smith

Morales

et al. 2017

Neuroscience Letters

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Although rodent models of traumatic brain injury (TBI) reliably produce cognitive and motor disturbances, behavioral characterization resulting from left and right hemisphere injuries remains unexplored. Here we examined the functional consequences of targeting the left versus right parietal cortex in lateral fluid percussion injury, on Morris water maze (MWM) spatial memory tasks (fixed platform and reversal) and neurological motor deficits (neurological severity score and rotarod). In the MWM fixed platform task, right lateral injury produced a small delay in acquisition rate compared to left. However, injury to either hemisphere resulted in probe trial deficits. In the MWM reversal task, left-right performance deficits were not evident, though left lateral injury produced mild acquisition and probe trial deficits compared to sham controls. Additionally, left and right injury produced similar neurological motor task deficits, impaired righting times, and lesion volumes. Injury to either hemisphere also produced robust ipsilateral, and modest contralateral, morphological changes in reactive microglia and astrocytes. In conclusion, left and right lateral TBI impaired MWM performance, with mild fixed platform acquisition rate differences, despite similar motor deficits, histological damage, and glial cell reactivity. Thus, while both left and right lateral TBI produce cognitive deficits, laterality in mouse MWM learning and memory merits consideration in the investigation of TBI-induced cognitive consequences.

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Section: Discussionsupporting

confidence: 84%

“…The left and right lateral injury deficits seen in the Fixed Platform probe trial are consistent with existing left [27] and right [30] lateral injury reference memory expression deficits. These results support findings that both hippocampal hemispheres contribute to spatial learning [30].…”

Section: Discussionsupporting

confidence: 81%

Investigation of left and right lateral fluid percussion injury in C57BL6/J mice: In vivo functional consequences

Schurman

Smith

Morales

et al. 2017

Neuroscience Letters

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“…We also found that high-frequency stimulationinduced LTP is only expressed at CA3-CA1 synapses when presynaptic input originates in the left CA3. Unilateral hippocampal lesions in mice have not revealed a distinct hemispheric contribution to long-term memory (25), although split-brain mice with left eye deprivation showed greater spatial memory accuracy than those with right eye deprivation when the environmental complexity increased (26). Studies in rats have either shown no effect of unilateral lesions (27,28) or no asymmetry of hippocampal function (27,29), or have produced inconsistent findings (30)(31)(32).…”

Section: Resultsmentioning

confidence: 99%

Left–right dissociation of hippocampal memory processes in mice

Shipton

El-Gaby

Apergis-Schoute

et al. 2014

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

163

222

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Left-right asymmetries have likely evolved to make optimal use of bilaterian nervous systems; however, little is known about the synaptic and circuit mechanisms that support divergence of function between equivalent structures in each hemisphere. Here we examined whether lateralized hippocampal memory processing is present in mice, where hemispheric asymmetry at the CA3-CA1 pyramidal neuron synapse has recently been demonstrated, with different spine morphology, glutamate receptor content, and synaptic plasticity, depending on whether afferents originate in the left or right CA3. To address this question, we used optogenetics to acutely silence CA3 pyramidal neurons in either the left or right dorsal hippocampus while mice performed hippocampus-dependent memory tasks. We found that unilateral silencing of either the left or right CA3 was sufficient to impair short-term memory. However, a striking asymmetry emerged in long-term memory, wherein only left CA3 silencing impaired performance on an associative spatial long-term memory task, whereas right CA3 silencing had no effect. To explore whether synaptic properties intrinsic to the hippocampus might contribute to this left-right behavioral asymmetry, we investigated the expression of hippocampal long-term potentiation. Following the induction of long-term potentiation by high-frequency electrical stimulation, synapses between CA3 and CA1 pyramidal neurons were strengthened only when presynaptic input originated in the left CA3, confirming an asymmetry in synaptic properties. The dissociation of hippocampal long-term memory function between hemispheres suggests that memory is routed via distinct left-right pathways within the mouse hippocampus, and provides a promising approach to help elucidate the synaptic basis of long-term memory. U nilateral specializations may facilitate greater processing power in bilateral brain structures by using the available neuronal circuitry more effectively. Nevertheless, the nature of the mechanisms that can act within the confines of duplicate neural structures to support different cognitive functions in each hemisphere remains elusive.The hippocampus is essential for certain forms of learning and memory, both in humans (1) and in rodents (2, 3), and also plays an important role in navigation (4). The left and right mammalian hippocampi comprise the same anatomical areas and directional connectivity, and yet in the human hippocampus, taskrelated activity may be localized to only one hemisphere (5). This lateralization may enable the left and right hippocampus to support complementary functions in human episodic memory, with left hippocampal activity associated with an egocentric, sequential representation of space but greater activity in the right hippocampus when an allocentric representation is used (6). It has been suggested that human hippocampal asymmetry is primarily dictated by external asymmetry-namely, the left hemispheric involvement in language processing and the stronger contribution of the right hemisphere to visuosp...

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“…Also in roll it was also increased more in the right fore limb in the diagonal back right direction, whereas the left limb did not respond similarly (Figure 2). Spatial processing is primarily in the right hemisphere (Shinohara et al, 2012). Stepping movements are presumed to represent subcortical startle reactions, as opposed to a reaction mediated by the cerebral cortex, which approximately halves the reaction time from 150 to 80 ms (Valls-Solé et al, 1999).…”

Section: Discussionmentioning

confidence: 99%