Morphological evidence for the sprouting of inhibitory commissural fibers in response to the lesion of the excitatory entorhinal input to the rat dentate gyrus

Recently a commissural fiber projection that terminates in the outer molecular layer of the fascia dentata was described in normal rats (Deller et al., 1995). In the present article, Phaseolus vulgaris leucoagglutinin (PHAL) tracing was used to analyze the contribution of this previously unknown projection to the commissural sprouting response after entorhinal cortex lesion. Rats 4–8 weeks after unilateral entorhinal lesion received a single PHAL deposit into the hilus of the fascia dentata contralateral to the lesion side. Unlesioned control animals received a similar PHAL deposit. The degree of axonal arborization and the bouton density per axon length were determined for individual PHAL-labeled commissural axons to the outer molecular layer of the dentate gyrus. A significant increase in both parameters was observed in the lesioned group. The PHAL-labeled commissural fibers established symmetric synapses in the denervated outer molecular layer. Postembedding immunocytochemistry indicated that some of these sprouting commissural fibers are GABAergic. Our findings provide morphological evidence for lamina-specific sprouting of an inhibitory commissural projection that normally terminates in the outer molecular layer. This suggests that inhibitory fibers participate in the replacement of the excitatory perforant pathway after entorhinal lesion.

[1]  T. Blackstad.  Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination , 1956, The Journal of comparative neurology.

[2]  G. Lynch,et al.  Time-dependent changes in commissural field potentials in the dentate gyrus following lesions of the entorhinal cortex in adult rats , 1975, Brain Research.

[3]  C. Cotman,et al.  Axonal transport and axon sprouting in the adult rat dentate gyrus: An autoradiographic study , 1980, Neuroscience.

[4]  T. Berger,et al.  Hippocampal polymorph neurons are the cells of origin for ipsilateral association and commissural afferents to the dentate gyrus , 1981, Brain Research.

[5]  O. Steward,et al.  The process of reinnervation in the dentate gyrus of the adult rat: A quantitative electron microscopic analysis of terminal proliferation and reactive synaptogenesis , 1983 .

[6]  Gary Lynch,et al.  An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts , 1976, Brain Research.

[7]  Gary Lynch,et al.  An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration , 1976, Brain Research.

[8]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[9]  J. Storm-Mathisen.  Choline acetyltransferase and acetylcholinesterase in fascia dentata following lesion of the entorhinal afferents. , 1974, Brain research.

[10]  S. Laurberg,et al.  Associational and commissural collaterals of neurons in the hippocampal formation (Hilus fasciae dentatae and subfield CA3) , 1981, Brain Research.

[11]  T. Hökfelt,et al.  Immunohistochemical demonstration of plasticity in GABA neurons of the adult rat dentate gyrus , 1982, Brain Research.

[12]  C. Geula,et al.  Anatomy of cholinesterase inhibition in Alzheimer's disease: Effect of physostigmine and tetrahydroaminoacridine on plaques and tangles , 1987, Annals of neurology.

[13]  M. Frotscher,et al.  Associational and commissural afferents of parvalbumin‐immunoreactive neurons in the rat hippocampus: A combined immunocytochemical and PHA‐L study , 1994, The Journal of comparative neurology.

[14]  O. Steward,et al.  Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: Recovery of alternation performance following unilateral entorhinal cortex lesions , 1977, Brain Research Bulletin.

[15]  J. Nadler.  Desensitization-like changes in GABA receptor binding of rat fascia dentata after entorhinal lesion , 1981, Neuroscience Letters.

[16]  M. Frotscher,et al.  Reorganization of input synapses of parvalbumin-containing neurons in the rat fascia dentata following entorhinal lesion , 1992, Neuroscience Letters.

[17]  M. Frotscher,et al.  Maintenance of peripheral dendrites of GABAergic neurons requires specific input , 1991, Brain Research.

[18]  G. Lynch,et al.  The effect of collateral sprouting on the density of innervation of normal target sites: implications for theories on the regulation of the size of developing synaptic domains , 1979, Brain Research.

[19]  T. M. Reeves,et al.  Reinnervation of the dentate gyrus and recovery of alternation behavior following entorhinal cortex lesions. , 1987, Behavioral neuroscience.

[20]  G. Lynch,et al.  The Hippocampus as a Model for Studying Anatomical Plasticity in the Adult Brain , 1975 .

[21]  O. Steward,et al.  Assessing the functional significance of lesion-induced neuronal plasticity. , 1982, International review of neurobiology.

[22]  J. Zimmer.  Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation , 1971, The Journal of comparative neurology.

[23]  O. Steward,et al.  Changes in the firing properties of neurons in the dentate gyrus with denervation and reinnervation: Implications for behavioral recovery , 1988, Experimental Neurology.

[24]  G. Lynch,et al.  Histochemical evidence of altered development of cholinergic fibers in the rat dentate gyrus following lesions: I. Time course after complete unilateral entorhinal lesion at various ages , 1977, The Journal of comparative neurology.

[25]  J. Zimmer,et al.  Extended commissural and ipsilateral projections in postnatally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. , 1973, Brain research.

[26]  S. Laurberg,et al.  Commissural and intrinsic connections of the rat hippocampus , 1979, The Journal of comparative neurology.

[27]  G. Lynch,et al.  Biochemical plasticity of short-axon interneurons: increased glutamate decarboxylase activity in the denervated area of rat dentate gyrus following entorhinal lesion. , 1974, Experimental neurology.

[28]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[29]  W. Cowan,et al.  Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  W. Cowan,et al.  An autoradiographic study of the organization of intrahippocampal association pathways in the rat , 1978, The Journal of comparative neurology.

[31]  M. Frotscher,et al.  Phaseolus vulgaris –leucoagglutinin tracing of commissural fibers to the rat dentate gyrus: Evidence for a previously unknown commissural projection to the outer molecular layer , 1995, The Journal of comparative neurology.

[32]  O. Steward.  Synapse Replacement on Cortical Neurons following Denervation , 1991 .

[33]  C. Nyakas,et al.  Changes in septo-hippocampal projections after lateral entorhinal or combined entorhinal-raphé lesions as studied by anterograde tracing methods , 1988, Brain Research Bulletin.

[34]  G. Lynch,et al.  Changes in the distribution of the dentate gyrus associational system following unilateral or bilateral entorhinal lesions in the adult rat , 1976, Brain Research.

[35]  D. Stein,et al.  Sparing and recovery of spatial alternation performance after entorhinal cortex lesions in rats , 1984, Behavioural Brain Research.

[36]  G. Lynch,et al.  Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat , 1975, Experimental Neurology.

[37]  O. Steward,et al.  Dendritic reorganization in the denervated dentate gyrus of the rat following entorhinal cortical lesions: A Golgi and electron microscopic analysis , 1983 .

[38]  G. Lynch,et al.  Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. , 1972, Brain research.

[39]  P. Somogyi,et al.  The Journal of Histochemistry and Cytochemistry Copyright Iii. Demonstration of Gaba in Golgi-impregnated Neurons and in Conventional Electron Microscopic Sections of Cat Striate Cortex' , 2022 .

[40]  W. Cowan,et al.  Autoradiographic studies of the commissural and ipsilateral association connection of the hippocampus and detentate gyrus of the rat. I. The commissural connections. , 1973, The Journal of comparative neurology.

[41]  O. Steward,et al.  Habituation-like decrements in transmission along the normal and lesion-induced temporodentate pathways in the rat , 1978, Brain Research.

[42]  G. Lynch,et al.  The effects of successive lesions on the time course of the sprouting response in the hippocampus of the rat , 1982, Brain Research.

[43]  J. West.  Age-dependent sprouting in the dentate gyrus demonstrated with anterograde HRP , 1984, Brain Research Bulletin.

[44]  G. Lynch,et al.  Developmental differences in post-lesion axonal growth in the hippocampus. , 1973, Brain research.

[45]  G. Lynch,et al.  A quantitative autoradiographic and electrophysiological study of the reinnervation of the dentate gyrus by the contralateral entorhinal cortex following ipsilateral entorhinal lesions , 1976, Brain Research.

[46]  W. Cowan,et al.  Autoradiographic studies of the commissural and ipsilateral association connections of the hippocampus and dentate gyrus. I. The commissural connections , 1973 .