Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions

Loesche, Jacquelyn; Steward, Oswald

doi:10.1016/0361-9230(77)90022-3

Cited by 230 publications

(84 citation statements)

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“…Given the discovery of cholinergic axonal sprouting in the hippocampus of patients with Alzheimer's disease (Geddes et al, 1985;Hyman et al, 1987), future studies exploring the functional significance of this cholinergic sprouting using gene delivery technologies similar to those used here may be well worth pursuing. Indeed, although the behavioral consequences of hippocampal reorganization are unclear in human beings, hippocampal sprouting of glutamatergic pathways in rats after unilateral entorhinal lesions has been shown to be beneficial in tests of mnemonic function (Loesche and Steward, 1977;Reeves and Smith, 1987;Ramirez et al, 1996). .…”

Section: Discussionmentioning

confidence: 99%

“…As previously described (Loesche and Steward, 1977), unilateral entorhinal lesions in the right hemisphere (i.e., ipsilateral to the rAAV injection) were made by lowering a stainless steel, insulated (except at the tip) electrode to the following stereotaxic coordinates: incisor bar set at Ϫ2.0 mm, 1.5 mm anterior to the transverse sinus; 3, 4, and 5 mm lateral to the sagittal sinus; and 2, 4, and 6 mm ventral to dura. A 1.0 mA current was passed through the electrode for a period of 45 sec at each coordinate (Ramirez and Stein, 1984).…”

Section: Methodsmentioning

confidence: 99%

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Adeno-Associated Virus Vector Expressing Nerve Growth Factor Enhances Cholinergic Axonal Sprouting after Cortical Injury in Rats

et al. 2003

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Nerve growth factor (NGF) is known to promote both the survival of cholinergic neurons after injury and the regeneration of damaged cholinergic axons. Recent evidence has implicated NGF in the regulation of cholinergic axonal sprouting by intact neurons projecting to the hippocampus of rats, sustaining a lesion of the entorhinal cortex. We explored the possibility that NGF may regulate this lesioninduced cholinergic sprouting by injecting recombinant adeno-associated virus (rAAV) vector expressing NGF and green fluorescent protein (GFP) into the dentate gyrus of rats that were subsequently given unilateral entorhinal lesions. Sprague Dawley rats were unilaterally injected with (1) rAAV vector expressing NGF and GFP or (2) rAAV vector expressing GFP. Fourteen days after injection, the animals received lesions of the entorhinal area ipsilateral to the virus injection. Four days after lesion, GFP expression and the septodentate sprouting response in the dentate gyrus were assessed. Optical densitometric analyses revealed a significant increase in acetylcholinesterase label (a marker for cholinergic septodentate sprouting) in the ipsilateral outer molecular layer of the dentate gyrus in rats injected with rAAV vector expressing NGF. Thus, NGF-expressing rAAV vector enhanced the sprouting response of intact cholinergic neurons after unilateral entorhinal lesions in rats.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Adeno-Associated Virus Vector Expressing Nerve Growth Factor Enhances Cholinergic Axonal Sprouting after Cortical Injury in Rats

et al. 2003

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“…Rats were subjected to UEC using the method of Loesche and Steward (1977). All animals were surgically prepared under isoflurane anesthesia delivered via nose cone (2% in carrier gas of 70% N 2 O and 30% O 2 ).…”

Section: Unilateral Entorhinal Cortex Lesionmentioning

confidence: 99%

Injury Modality, Survival Interval, and Sample Region Are Critical Determinants of qRT-PCR Reference Gene Selection during Long-Term Recovery from Brain Trauma

Harris

Reeves

Phillips

2009

Journal of Neurotrauma

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In the present study we examined expression of four real-time quantitative RT-PCR reference genes commonly applied to rodent models of brain injury. Transcripts for b-actin, cyclophilin A, GAPDH, and 18S rRNA were assessed at 2-15 days post-injury, focusing on the period of synaptic recovery. Diffuse moderate central fluid percussion injury (FPI) was contrasted with unilateral entorhinal cortex lesion (UEC), a model of targeted deafferentation. Expression in UEC hippocampus, as well as in FPI hippocampus and parietotemporal cortex was analyzed by qRT-PCR. Within-group variability of gene expression was assessed and change in expression relative to paired controls was determined. None of the four common reference genes tested was invariant across brain region, survival time, and type of injury. Cyclophilin A appeared appropriate as a reference gene in UEC hippocampus, while b-actin was most stable for the hippocampus subjected to FPI. However, each gene may fail as a suitable reference with certain test genes whose RNA expression is targeted for measurement. In FPI cortex, all reference genes were significantly altered over time, compromising their utility for time-course studies. Despite such temporal variability, certain genes may be appropriate references if limited to single survival times. These data provide an extended baseline for identification of appropriate reference genes in rodent studies of recovery from brain injury. In this context, we outline additional considerations for selecting a qRT-PCR normalization strategy in such studies. As previously concluded for acute post-injury intervals, we stress the importance of reference gene validation for each brain injury paradigm and each set of experimental conditions.

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“…This produces a well-characterized pattern of synaptic reorganization confined to the distal two-thirds of the molecular layer, which corresponds to the outer molecular layer (OML), where EC inputs terminate (Steward, 1976). The pattern of synaptic reorganization includes a period of massive (ϳ90%) synapse loss (Matthews et al, 1976;Steward and Vinsant, 1983), followed by a period of terminal proliferation (sprouting) of excitatory afferents from commissural /associational pathways (Zimmer, 1973) and the contralateral EC (Steward et al, 1974), and reactive synaptogenesis (Steward and Vinsant, 1983) culminating in a degree of physiological and behavioral recovery (Loesche and Steward, 1977;Reeves and Smith, 1987;Reeves and Steward, 1988). Thus, this paradigm allows investigation of receptor changes during terminal degeneration and subsequent sprouting within spatially restricted segments of dendrites.…”

Section: Abstract: Excitatory Amino Acid Receptors; Immunocytochemismentioning

confidence: 99%

“…Both physiological and behavioral recovery (Loesche and Steward, 1977;Reeves and Smith, 1987) from unilateral EC lesions have been documented to occur during the time period examined. From these studies, it was hypothesized that the early phase of physiological recovery, before the major onset of new synapse formation, may be the result of an increase in the number of receptors, producing an increase in the activity of surviving synapses similar to denervation supersensitivity in muscle fibers .…”

Section: Functional Significancementioning

confidence: 99%

Differential Subcellular Regulation of NMDAR1 Protein and mRNA in Dendrites of Dentate Gyrus Granule Cells after Perforant Path Transection

Gazzaley¹,

Benson²,

Huntley³

et al. 1997

J. Neurosci.

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Unilateral transection of the excitatory perforant path results in the acute deafferentation of a segregated zone on the distal dendrites of hippocampal dentate gyrus granule cells (i.e., outer molecular layer), followed by sprouting, reactive synaptogenesis, and a return of physiological and behavioral function. To investigate cellular mechanisms underlying NMDA receptor plasticity in response to such extensive synaptic reorganization, we quantitatively evaluated changes in intensity levels of NMDAR1 immunofluorescence and NMDAR1 mRNA hybridization within subcellular compartments of dentate gyrus granule cells 2, 5, and 9 d after perforant path lesions. There were no significant changes in either measure at 2 d postlesion. However, at 5 and 9 d postlesion, during the period of axonal sprouting and synaptogenesis, there was an increase in NMDAR1 immunolabeling that was restricted to the dendritic segments of the denervated outer molecular layer and the granule cell somata. In contrast, NMDAR1 mRNA levels at 5 and 9 d postlesion increased throughout the full extent of the molecular layer, including both denervated and nondenervated segments of granule cell dendrites. These findings reveal that NMDAR1 mRNA is one of a limited population of mRNAs that is transported into dendrites and further suggest that in response to terminal proliferation and sprouting, increased mRNA transport occurs throughout the full dendritic extent, whereas increased local protein synthesis is restricted to denervated regions of the dendrites whose afferent activity is perturbed. These results begin to elucidate the dynamic postsynaptic subcellular regulation of receptor subunits associated with synaptic plasticity after denervation.

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Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions

Cited by 230 publications

References 20 publications

Adeno-Associated Virus Vector Expressing Nerve Growth Factor Enhances Cholinergic Axonal Sprouting after Cortical Injury in Rats

Adeno-Associated Virus Vector Expressing Nerve Growth Factor Enhances Cholinergic Axonal Sprouting after Cortical Injury in Rats

Injury Modality, Survival Interval, and Sample Region Are Critical Determinants of qRT-PCR Reference Gene Selection during Long-Term Recovery from Brain Trauma

Differential Subcellular Regulation of NMDAR1 Protein and mRNA in Dendrites of Dentate Gyrus Granule Cells after Perforant Path Transection

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