Associative long-term potentiation in piriform cortex slices requires GABAA blockade

Previous studies have demonstrated that NMDA-dependent, long-term potentiation (LTP) can be induced in both afferent and intrinsic association fiber systems in the piriform (primary olfactory) cortex. In this report we demonstrate that an associative form of LTP can be induced by coactivation of these two systems, which terminate on adjacent apical dendritic segments of pyramidal cells. Potentiating stimulus trains were delivered to either afferent or association fibers, and weak shocks, which were nonpotentiating when delivered alone, were delivered to the other pathway. Under control recording conditions where homosynaptic (single pathway) LTP is consistently evoked, coincident application of these stimuli failed to induce LTP of the weak shock response. However, after local blockade of the fast, GABAA-mediated IPSP, associative LTP was consistently produced in both directions. Induction was blocked by D-2-amino-5-phosphonovaleric acid, indicating that it is dependent on activation of NMDA receptors. It is speculated that afferent and association fibers are segregated on different dendritic segments of pyramidal cells in piriform cortex to allow regulation of associative LTP by way of centrifugal inputs that modulate the activity of GABAergic interneurons.

[1]  W B Levy,et al.  Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. , 1990, Journal of neurophysiology.

[2]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  D. Lewis,et al.  Facilitation of the induction of long-term potentiation by GABAB receptors , 1991, Science.

[4]  J Ambros-Ingerson,et al.  Simulation of paleocortex performs hierarchical clustering. , 1990, Science.

[5]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[6]  B. Gustafsson,et al.  Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  T. H. Brown,et al.  Associative long-term potentiation in hippocampal slices. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[8]  J. Price An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex , 1973, The Journal of comparative neurology.

[9]  H. Scharfman,et al.  Selective depression of GABA-mediated IPSPs by somatostatin in area CA1 of rabbit hippocampal slices , 1989, Brain Research.

[10]  R. Traub,et al.  Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. , 1988, Journal of neurophysiology.

[11]  G. Lynch,et al.  Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation , 1986, Brain Research.

[12]  T. A. Pitler,et al.  Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. , 1992, The Journal of physiology.

[13]  R. Nicoll,et al.  Comparison of the action of baclofen with gamma‐aminobutyric acid on rat hippocampal pyramidal cells in vitro. , 1985, The Journal of physiology.

[14]  T. Dunwiddie,et al.  Differential effects of mu‐ and delta‐receptor selective opioid agonists on feedforward and feedback GABAergic inhibition in hippocampal brain slices , 1991, Synapse.

[15]  G. Lynch,et al.  Long-term potentiation of monosynaptic EPSPs in rat piriform cortex in vitro. , 1990, Synapse.

[16]  D. Madison,et al.  Synaptic localization of adrenergic disinhibition in the rat hippocampus , 1991, Neuron.

[17]  L. Haberly Neuronal circuitry in olfactory cortex: anatomy and functional implications , 1985 .

[18]  C. Scholfield A depolarizing inhibitory potential in neurones of the olfactory cortex in vitro. , 1978, The Journal of physiology.

[19]  H. Eichenbaum,et al.  Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  L. Haberly,et al.  NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro , 1990, Brain Research.

[21]  B. R. Sastry,et al.  Associative induction of posttetanic and long-term potentiation in CA1 neurons of rat hippocampus. , 1986, Science.

[22]  R K Wong,et al.  Synchronized burst discharge in disinhibited hippocampal slice. II. Model of cellular mechanism. , 1983, Journal of neurophysiology.

[23]  N. Ropert,et al.  Serotonin facilitates GABAergic transmission in the CA1 region of rat hippocampus in vitro. , 1991, The Journal of physiology.

[24]  K. Mori,et al.  Two types of postsynaptic inhibition in pyriform cortex of the rabbit: fast and slow inhibitory postsynaptic potentials. , 1982, Journal of Neurophysiology.

[25]  M. Andreasen,et al.  Noradrenaline receptors participate in the regulation of GABAergic inhibition in area CA1 of the rat hippocampus. , 1991, The Journal of physiology.

[26]  H. Wigström,et al.  Hippocampal long-term potentiation is induced by pairing single afferent volleys with intracellularly injected depolarizing current pulses. , 1986, Acta physiologica Scandinavica.

[27]  H. Wigström,et al.  Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition , 1983, Nature.

[28]  J. Bower,et al.  Olfactory cortex: model circuit for study of associative memory? , 1989, Trends in Neurosciences.

[29]  G. Collingridge,et al.  GABAB autoreceptors regulate the induction of LTP , 1991, Nature.

[30]  L. Haberly,et al.  Characterization of synaptically mediated fast and slow inhibitory processes in piriform cortex in an in vitro slice preparation. , 1988, Journal of neurophysiology.

[31]  H. Wigström,et al.  Facilitation of hippocampal long-lasting potentiation by GABA antagonists. , 1985, Acta physiologica Scandinavica.

[32]  Matthew A. Wilson,et al.  A Computer Simulation of Olfactory Cortex with Functional Implications for Storage and Retrieval of Olfactory Information , 1987, NIPS.

[33]  R. Nicoll,et al.  Mechanisms underlying long-term potentiation of synaptic transmission. , 1991, Annual review of neuroscience.