Potassium-induced epileptiform activity in area CA3 varies markedly along the septotemporal axis of the rat hippocampus

Bragdon, Andrew; Taylor, Donald M.; Wilson, Wilkie A.

doi:10.1016/0006-8993(86)90300-8

Cited by 107 publications

(71 citation statements)

References 18 publications

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“…Greater spontaneous epileptiform bursting in VH than DH 15,182 . Human • Chronic intracranial recordings in patients indicate seizure initiation more frequent from AH than PH 183 .…”

Section: Animalmentioning

confidence: 88%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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The precise functional role of the hippocampus remains a topic of much debate. According to a dominant view, the dorsal/posterior hippocampus is implicated in memory and spatial navigation and the ventral/anterior hippocampus mediates anxietyrelated behaviours. However, this 'dichotomy view' may need revision. Gene expression studies demonstrate multiple functional domains along the hippocampal long axis, which often exhibit sharply demarcated borders. By contrast, anatomical studies and electrophysiological recordings in rodents suggest that the long-axis is organized along a gradient. Together, these observations suggest a model in which functional long-axis gradients are superimposed on discrete functional domains. This model provides a potential framework to explain and test the multiple functions ascribed to the hippocampus.The hippocampus is a medial temporal lobe structure critically involved in episodic memory and spatial navigation [1][2][3][4][5][6][7] . Its long, curved form is present across all mammalian orders and runs along a dorsal (septal) to ventral (temporal) axis in rodents, corresponding to a posteriorto-anterior axis in humans (FIG. 1a-b). The same basic intrinsic circuitry is maintained throughout the long axis and across species (FIG. 1c). Despite this conserved intrinsic circuitry, the dorsal and ventral portions have different connectivities with cortical and subcortical areas, and this has long posed a question as to whether the hippocampus is functionally uniform along this axis. Here we review cross-species data that show how the seemingly disparate functions ascribed to the hippocampus can be accommodated by a model in which different functional properties exist along the longitudinal axis.The severe memory impairment suffered by patient H.M. following bilateral hippocampal resection 1 led to intensive study 8 of patients and animal models with hippocampal damage, with an ensuing characterisation of hippocampal function in terms of declarative memory 2 , encompassing both episodic and semantic memory. At the same time, however, evidence emerged for a hippocampal role in spatial memory, based on the discovery of hippocampal 'place cells' 9,10 and the demonstration that hippocampal lesions impair spatial memory 4 . Both the declarative memory hypothesis 11 and the spatial mapping hypothesis 12 of hippocampal function proposed a unitary model in which the entire hippocampus is dedicated

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“…Greater spontaneous epileptiform bursting in VH than DH 15,182 . Human • Chronic intracranial recordings in patients indicate seizure initiation more frequent from AH than PH 183 .…”

Section: Animalmentioning

confidence: 88%

Functional organization of the hippocampal longitudinal axis

Witter²,

et al. 2014

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“…Mean amplitude of evoked potentials is higher in slices taken from the temporal pole of the hippocampus at baseline conditions (Gilbert et al 1985;Maggio and Segal 2007). At higher K þ concentrations, epileptiform bursting was induced in all slices, but there was a higher likelihood of burst firing in temporal slices as compared with septal ones (Gilbert et al 1985;Bragdon et al 1986). In contrast, the threshold for long-term potentiation (LTP) induction appears to be lower in slices taken from the septal pole of CA1 (Elul 1964).…”

Section: Electrophysiological Propertiesmentioning

confidence: 95%

Functional Differentiation of Adult-Born Neurons along the Septotemporal Axis of the Dentate Gyrus: Figure 1.

Sahay

Duman

et al. 2015

Cold Spring Harb Perspect Biol

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Over the past several decades, the proliferation and integration of adult-born neurons into existing hippocampal circuitry has been implicated in a wide range of behaviors, including novelty recognition, pattern separation, spatial learning, anxiety behaviors, and antidepressant response. In this review, we suggest that the diversity in behavioral requirements for new neurons may be partly caused by separate functional roles of individual neurogenic niches. Growing evidence shows that the hippocampal formation can be compartmentalized not only along the classic trisynaptic circuit, but also along a longitudinal septotemporal axis. We suggest that subpopulations of hippocampal adult-born neurons may be specialized for distinct mnemonic-or mood-related behavioral tasks. We will examine the literature supporting a functional and anatomical dissociation of the hippocampus along the longitudinal axis and discuss techniques to functionally dissect the roles of adult-born hippocampal neurons in these distinct subregions.

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“…The electrophysiological differences of hippocampal slices from kainate-and pilocarpine-treated rats compared to H-I animals may also arise from inherent differences in septal hippocampal slices (i.e., H-I rats) versus the temporal hippocampus (i.e., kainate-and pilocarpine-treated rats). Differences between the septal and temporal hippocampus in the rate of kindling and frequency of spontaneous bursting in CA3 have suggested that the temporal hippocampus is more prone to epileptiform activity (Racine et al, 1977;Bragdon et al, 1986). Mechanisms other than mossy fiber sprouting in the IML and the formation of new recurrent excitatory synapses, such as the formation of new excitatory synapses with basilar dendrites (Ribak et al, 2000) and alterations in glutamate receptors (Mathern et al, 1996), could also contribute to the abnormal electrophysiological responses seen after H-I injury.…”

Section: Evidence For New Recurrent Excitatory Circuitsmentioning

confidence: 99%

A chronic histopathological and electrophysiological analysis of a rodent hypoxic–ischemic brain injury model and its use as a model of epilepsy

Williams¹,

Dudek

2007

Neuroscience

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Ischemic brain injury is one of the leading causes of epilepsy in the elderly, and there are currently no adult rodent models of global ischemia, unilateral hemispheric ischemia, or focal ischemia that report the occurrence of spontaneous motor seizures following ischemic brain injury. The rodent hypoxic-ischemic (H-I) model of brain injury in adult rats is a model of unilateral hemispheric ischemic injury. Recent studies have shown that an H-I injury in perinatal rats causes hippocampal mossy fiber sprouting and epilepsy. These experiments aimed to test the hypothesis that a unilateral H-I injury leading to severe neuronal loss in young-adult rats also causes mossy fiber sprouting and spontaneous motor seizures many months after the injury, and that the mossy fiber sprouting induced by the H-I injury forms new functional recurrent excitatory synapses. The right common carotid artery of 30-day old rats was permanently ligated, and the rats were placed into a chamber with 8% oxygen for 30 min. A quantitative stereologic analysis revealed that the ipsilateral hippocampus had significant hilar and CA1 neuronal loss compared to the contralateral and sham-control hippocampi. The septal region from the ipsilateral and contralateral hippocampus had small but significantly increased amounts of Timm staining in the inner molecular layer compared to the sham-control hippocampi. Three of 20 lesioned animals (15%) were observed to have at least one spontaneous motor seizure 6-12 months after treatment. Approximately 50% of the ipsilateral and contralateral hippocampal slices displayed abnormal electrophysiological responses in the dentate gyrus, manifest as all-or-none bursts to hilar stimulation. This study suggests that H-I injury is associated with synaptic reorganization in the lesioned region of the hippocampus, and that new recurrent excitatory circuits can predispose the hippocampus to abnormal electrophysiological activity and spontaneous motor seizures. KeywordsEpilepsy; sprouting; recurrent excitation; population spikes; epileptiform bursts Correspondence to: F. Edward Dudek, Ph.D. Department of Physiology, University of Utah School of Medicine, 420 Chipeta Way, Suite 1700, Salt Lake City, UT 84108, (801) 587-5880, ed.dudek@hsc.utah.edu. 1 Current address: Department of Neurosciences, Case Western Reserve University School of Medicine, Cleveland, OH; 2 Current address: Department of Physiology, University of Utah School of Medicine, Salt Lake City, UT.Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Author ManuscriptNeuroscience. Author manuscript; ...

show abstract

Potassium-induced epileptiform activity in area CA3 varies markedly along the septotemporal axis of the rat hippocampus

Cited by 107 publications

References 18 publications

Functional organization of the hippocampal longitudinal axis

Functional organization of the hippocampal longitudinal axis

Functional Differentiation of Adult-Born Neurons along the Septotemporal Axis of the Dentate Gyrus: Figure 1.

A chronic histopathological and electrophysiological analysis of a rodent hypoxic–ischemic brain injury model and its use as a model of epilepsy

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