All Layers of Medial Entorhinal Cortex Receive Presubicular and Parasubicular Inputs

Canto, Cathrin B.; Koganezawa, Noriko; Beed, Prateep; Moser, Edvard I; Witter, Menno P.

doi:10.1523/jneurosci.3526-12.2012

Cited by 55 publications

(62 citation statements)

References 55 publications

(3 reference statements)

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“…In line with the above, proposed architecture mediating superficial to deep intrinsic connectivity in MEC, PrS and PaS inputs contact layer V pyramidal neurons on their apical dendrites [83]. We recently showed electrophysiologically that principal neurons in all layers of MEC receive convergent monosynaptic inputs from both PaS and PrS (figure 3) [34]. These shared inputs thus provide a parsimonious substrate for the prominent directional tuning of head-direction cells and the coherent orientational tuning of grid cells in all layers of MEC.…”

Section: Grid Cells and Head-direction Cellssupporting

confidence: 68%

Architecture of spatial circuits in the hippocampal region

Witter

Canto

Couey

et al. 2014

Phil. Trans. R. Soc. B

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The hippocampal region contains several principal neuron types, some of which show distinct spatial firing patterns. The region is also known for its diversity in neural circuits and many have attempted to causally relate network architecture within and between these unique circuits to functional outcome. Still, much is unknown about the mechanisms or network properties by which the functionally specific spatial firing profiles of neurons are generated, let alone how they are integrated into a coherently functioning meta-network. In this review, we explore the architecture of local networks and address how they may interact within the context of an overarching space circuit, aiming to provide directions for future successful explorations.

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Section: Grid Cells and Head-direction Cellssupporting

confidence: 68%

Architecture of spatial circuits in the hippocampal region

Witter

Canto

Couey

et al. 2014

Phil. Trans. R. Soc. B

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“…Our data suggest that PrS contributes significantly to synaptic inhibition of LII stellate cells in the MEA. This contribution could either be directly through GABAergic projecting neurons (Canto et al 2012;Tolner et al 2007), and/or via afferents to local interneurons within MEA that mediate feed-forward inhibition of neurons in layers II and III (Canto et al 2012;Tolner et al 2007;van Haeften et al 1997). The reduced inhibitory synaptic drive noted in LII stellate cells under epileptic conditions (Kobayashi et al 2003;Kumar et al 2007;Tolner et al 2007) is consistent with diminution of PrS-mediated synaptic inhibition arising in part from either loss of GABAergic neurons in PrS, including MEA-targeting projection neurons (Drexel et al 2012;van Vliet et al 2004), loss of local GABAergic interneurons in MEA (Kumar and Buckmaster 2006;van Vliet et al 2004) and/or downregulation of GABA subunits mediating tonic inhibition (Drexel et al 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Anatomical studies have posited that projections from deep-layer neurons within the MEA provide direct excitatory input to and support feed-forward inhibition of superficial-layer neurons (Gloveli et al 2001;van Haeften et al 2003) and are of importance to MEA function (Dickson et al 2000;Kloosterman et al 2003a). Furthermore, deep-layer neurons receive input directly from PrS and the parasubiculum (Bartesaghi et al 2005;Canto et al 2012;Tolner et al 2007), and together may be of significance in propagating aberrant activity to superficial layers under conditions of enhanced excitability (Dickson and Alonso 1997;Lopantsev and Avoli 1998;Stewart 1999). A possible explanation for why we did not see a reduction in frequency of postsynaptic currents in LIII pyramidal neurons following focal application of NBQX to PrS relates to our previous observation that excitatory drive to RS cells, the predominant cell type in PrS, is significantly reduced under epileptic conditions and comprises mostly non-action potential dependent events (Abbasi and Kumar 2014).…”

Section: Discussionmentioning

confidence: 99%

“…The cut dorsal surface of the brain was adhered to the cutting platform using cyanoacrylate glue. We chose this cutting angle to increase the likelihood of preserving PrS projections to MEA in acute brain slices (Canto et al 2012;Tolner et al 2007), because PrS projections tend to travel to the MEA in a lateroventral orientation (Honda and Ishizuka 2004). Semihorizontal slices (400 m) were prepared using a microslicer (VT1000S, Leica, Germany) in the chilled cutting solution and allowed to equilibrate in oxygenated artificial cerebrospinal fluid (aCSF) containing (in mM) 126 NaCl, 26 NaHCO 3 , 3 KCl, 1.25 NaH 2 PO 4 , 2 MgSO 4 , 2 CaCl 2 , 0.25 L-glutamine, and 10 D-glucose (pH 7.4), first at 32°C for 1 h and subsequently at room temperature before being transferred to the recording chamber.…”

Section: Methodsmentioning

confidence: 99%

“…The presubiculum, which provides an anatomically robust and functionally significant input to the MEA (Boccara et al 2010;Canto et al 2012;Kononenko and Witter 2012), that is both glutamatergic and GABAergic in nature (van Haeften et al 1997), terminating predominantly in LI and LIII (Caballero-Bleda and Witter 1993), is of particular interest to TLE pathophysiology. Previous studies in which rats were made epileptic using the kainate model (Tolner et al 2007;Tolner et al 2005) or aminooxyacetic acid (Scharfman et al 1998) suggest that PrS stimulation can drive hyperexcitability of superficial MEA neurons and changes in functional network connectivity with MEA enables PrS to promote epileptiform activity in the superficial layers.…”

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confidence: 99%

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Layer-specific modulation of entorhinal cortical excitability by presubiculum in a rat model of temporal lobe epilepsy

Abbasi

Kumar

2015

Journal of Neurophysiology

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Abbasi S, Kumar SS. Layer-specific modulation of entorhinal cortical excitability by presubiculum in a rat model of temporal lobe epilepsy. J Neurophysiol 114: 2854 -2866, 2015. First published September 16, 2015 doi:10.1152/jn.00823.2015 is the most common form of epilepsy in adults and is often refractory to antiepileptic medications. The medial entorhinal area (MEA) is affected in TLE but mechanisms underlying hyperexcitability of MEA neurons require further elucidation. Previous studies suggest that inputs from the presubiculum (PrS) contribute to MEA pathophysiology. We assessed electrophysiologically how PrS influences MEA excitability using the rat pilocarpine model of TLE. PrS-MEA connectivity was confirmed by electrically stimulating PrS afferents while recording from neurons within superficial layers of MEA. Assessment of alterations in PrS-mediated synaptic drive to MEA neurons was made following focal application of either glutamate or NBQX to the PrS in control and epileptic animals. Here, we report that monosynaptic inputs to MEA from PrS neurons are conserved in epileptic rats, and that PrS modulation of MEA excitability is layer-specific. PrS contributes more to synaptic inhibition of LII stellate cells than excitation. Under epileptic conditions, stellate cell inhibition is significantly reduced while excitatory synaptic drive is maintained at levels similar to control. PrS contributes to both synaptic excitation and inhibition of LIII pyramidal cells in control animals. Under epileptic conditions, overall excitatory synaptic drive to these neurons is enhanced while inhibitory synaptic drive is maintained at control levels. Additionally, neither glutamate nor NBQX applied focally to PrS now affected EPSC and IPSC frequency of LIII pyramidal neurons. These layer-specific changes in PrS-MEA interactions are unexpected and of significance in unraveling pathophysiological mechanisms underlying TLE. temporal lobe epilepsy; presubiculum; glutamate application; hyperexcitability; electrophysiology TEMPORAL LOBE EPILEPSY (TLE) is characterized by spontaneous recurrent seizures emanating from temporal lobe foci. It is the most common form of epilepsy in adults, and is often associated with drug-resistant seizures (Engel 1998;Engel et al. 2008).

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Electrophysiological and morphological characterization of cells in superficial layers of rat presubiculum

Abbasi

Kumar

2013

J of Comparative Neurology

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The presubiculum (PrS) plays critical roles in spatial information processing and memory consolidation and has also been implicated in temporal lobe epileptogenesis. Despite its involvement in these processes, a basic structure-function analysis of PrS cells remains far from complete. To this end, we performed whole-cell recording and biocytin labeling of PrS neurons in layer (L)II and LIII to examine their electrophysiological and morphological properties. We characterized the cell types based on electrophysiological criteria, correlated their gross morphology, and classified them into distinct categories using unsupervised hierarchical cluster analysis. We identified seven distinct cell types: regular-spiking (RS), irregular-spiking (IR), initially bursting (IB), stuttering (Stu), single-spiking (SS), fast-adapting (FA), and late-spiking (LS) cells, of which RS and IB cells were common to LII and LIII, LS cells were specific to LIII, and the remaining types were identified exclusively in LII. Recorded neurons were either pyramidal or nonpyramidal and, except for Stu cells, displayed spine-rich dendrites. The RS, IB, and IR cells appeared to be projection neurons based on extension of their axons into LIII of the medial entorhinal area (MEA) and/or angular bundle. We conclude that LII and LIII of PrS are distinct in their neuronal populations and together constitute a more diverse population of neurons than previously suggested. PrS neurons serve as major drivers of circuits in superficial (LII-III) entorhinal cortex (ERC) and couple neighboring structures through robust afferentation, thereby substantiating the PrS's critical role in the parahippocampal region.

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All Layers of Medial Entorhinal Cortex Receive Presubicular and Parasubicular Inputs

Cited by 55 publications

References 55 publications

Architecture of spatial circuits in the hippocampal region

Architecture of spatial circuits in the hippocampal region

Layer-specific modulation of entorhinal cortical excitability by presubiculum in a rat model of temporal lobe epilepsy

Electrophysiological and morphological characterization of cells in superficial layers of rat presubiculum

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