Long-term potentiation and depression of synaptic transmission in rat posterior cingulate cortex

We used stimulation of corpus callosum (CAL) and the subiculo-cingulate tract (SCT), in an in vitro brain slice preparation, to study activity-dependent changes in synaptic efficacy in posterior cingulate cortex (PCC). SCT stimulation monosynaptically excites the apical dendrites of deep laminae (V-VI) pyramidal neurons, while CAL afferents drive these same cells via synapses on their basal dendrites. In contrast, most superficial laminae (II/III-IV) pyramids appear to be driven polysynaptically via ascending axonal collaterals of deep pyramids. In slices retaining these connectivities, we contrasted characteristics of synaptic plasticity in superficial vs deep laminae field and intracellular potentials evoked by conditioning stimuli given at frequencies of 100, 20, 8, 5 and 1 Hz. Tetanic stimulation (100 Hz) of SCT or CAL yielded homosynaptic long-term potentiation (LTP) of each pathway, while stimulus trains of 8-20 Hz did not. 1-5 Hz stimulation of SCT and CAL elicited homosynaptic long-term depression (LTD) of synaptic strength in each pathway. Associative LTD was induced by interleaving 5 Hz pulses to the SCT pathway with 100 Hz theta-burst stimulation of CAL, but was not induced when these stimulus loci were switched. Heterosynaptic non-associative LTD was also observed in the alternate pathway following tetanization of either SCT or CAL. In all cases, LTP and LTD were observed only in deep laminae recordings. In contrast, superficial records showed only paired-pulse facilitation and short-term post-tetanic potentiation. In in vivo experiments in anaesthetized rats, PCC responses to SCT stimulation were contrasted with responses to stimulation of anteroventral and anterodorsal thalamic nuclei (AV/AD). SCT-elicited field potentials closely resembled those evoked in the slice, with maximal amplitude tuned to the 4-8 Hz frequency band. AV/AD stimulation elicited field potentials which were not frequency tuned. Overall, these data suggest that the acute circuit properties of PCC superficial laminae, modulated by thalamic input and synaptic plasticity in deep laminae, can transform hippocampal synaptic inflow before relaying it to extracingulate targets.

[1]  M. Gabriel,et al.  Interaction of laminae of the cingulate cortex with the anteroventral thalamus during behavioral learning. , 1980, Science.

[2]  G. V. Simpson,et al.  Microcircuitry of posterior cingulate cortex in vitro: electrophysiology and laminar analysis using the current source density method , 1993, Brain Research.

[3]  M. Bear,et al.  Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. , 1993, Science.

[4]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[5]  G. Buzsáki.  Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[6]  K. Horikawa,et al.  Topographic organization and collateralization of the projections of the anterior and laterodorsal thalamic nuclei to cingulate areas 24 and 29 in the rat , 1988, Neuroscience Research.

[7]  Nobuaki Tamamaki,et al.  Columnar organization in the subiculum formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1987, Brain Research.

[8]  C. Saper.  Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus , 1984, The Journal of comparative neurology.

[9]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[10]  E. W. Powell,et al.  The cingulate bridge between allocortex, isocortex and thalamus , 1978, The Anatomical record.

[11]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Babb,et al.  Afferent fibers to rat cingulate cortex , 1984, Experimental Neurology.

[13]  H. Swadlow,et al.  Efferent systems of the rabbit visual cortex: Laminar distribution of the cells of origin, axonal conduction velocities, and identification of axonal branches , 1981, The Journal of comparative neurology.

[14]  N. Schmajuk.  Psychological theories of hippocampal function , 1984 .

[15]  H. Haas,et al.  A simple perfusion chamber for the study of nervous tissue slices in vitro , 1979, Journal of Neuroscience Methods.

[16]  C. H. Vanderwolf,et al.  Hippocampal Rhythmic Slow Activity and Neocortical Low-Voltage Fast Activity: Relations to Behavior , 1975 .

[17]  P. Stanton,et al.  Priming of homosynaptic long-term depression in hippocampus by previous synaptic activity. , 1993, Neuroreport.

[18]  T. Sejnowski,et al.  Commissural synapses, but not mossy fiber synapses, in hippocampal field CA3 exhibit associative long-term potentiation and depression , 1989, Brain Research.

[19]  D. Powell,et al.  Cingulate cortex: its role in Pavlovian conditioning. , 1982, Journal of comparative and physiological psychology.

[20]  Post‐tetanic potentiation of twitch motor units in snake costocutaneous muscle. , 1978, The Journal of physiology.

[21]  C. H. Vanderwolf,et al.  Pathways through cingulate, neo-and entorhinal cortices mediate atropine-resistant hippocampal rhythmical slow activity , 1985, Brain Research.

[22]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[23]  Alan Peters,et al.  Synaptic termination of thalamic and callosal afferents in cingulate cortex of the rat , 1981, The Journal of comparative neurology.

[24]  W. Abraham,et al.  Priming of associative long-term depression in the dentate gyrus by θ frequency synaptic activity , 1992, Neuron.

[25]  T. Babb,et al.  Excitatory projection of the rat subicular complex to the cingulate cortex and synaptic integration with thalamic afferents , 1984, Brain Research.

[26]  A. Siegel,et al.  Subicular projections to the posterior cingulate cortex in rats , 1977, Experimental Neurology.

[27]  M. Wiesendanger,et al.  The corticopontine system in the rat. II. The projection pattern , 1982, The Journal of comparative neurology.

[28]  J. Kaas.  The organization of neocortex in mammals: implications for theories of brain function. , 1987, Annual review of psychology.

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

[30]  J. E. Vaughn,et al.  Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex , 1983, Journal of neurocytology.

[31]  J. Borst,et al.  Electrical activity of the cingulate cortex. I. Generating mechanisms and relations to behavior , 1987, Brain Research.

[32]  M. Gabriel,et al.  Posterior cingulate cortical lesions eliminate learning-related unit activity in the anterior cingulate cortex , 1987, Brain Research.

[33]  G. Lynch,et al.  Long‐term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. , 1978, The Journal of physiology.

[34]  B. Vogt,et al.  Form and distribution of neurons in rat cingulate cortex: Areas 32, 24, and 29 , 1981, The Journal of comparative neurology.

[35]  Michael W. Miller,et al.  Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices , 1983, The Journal of comparative neurology.

[36]  T. Sejnowski,et al.  Associative long-term depression in the hippocampus induced by hebbian covariance , 1989, Nature.

[37]  M Mishkin,et al.  The origin, course, and termination of the hippocampothalamic projections in the macaque , 1986, The Journal of comparative neurology.

[38]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[39]  P. Greengard,et al.  Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons , 1991, Science.

[40]  F. L. D. Silva,et al.  Organization of the reciprocal connections between the subiculum and the enthorhinal cortex in the cat: II. An electrophysiological study , 1986, The Journal of comparative neurology.

[41]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.