Feedforward inhibition of the rat entorhinal cortex and subicular complex

We used in vivo intracellular recording techniques in order to provide evidence about the source of postsynaptic inhibition in the rat entorhinal cortex and subicular complex. Several different structures in the basal forebrain and hippocampus were electrically stimulated in order to activate inhibition by different pathways. This allowed a test of 2 different neuronal circuit models: feedback inhibition, in which recurrent collaterals from principal cell axons excite a local population of inhibitory neurons, and feedforward inhibition, in which excitatory afferents activate the inhibitory neurons. In both models, inhibitory cell axons branch and contribute to the inhibition of a population of principal cells. In the feedback model, a good correlation between antidromic and inhibitory response latencies is predicted. The feedforward model predicts independent antidromic and inhibitory response latencies. In one particular model of feedforward inhibition, afferents excite both local inhibitory cells and principal cells. This model predicts a high correlation between principal cell EPSP and IPSP latencies. The results showed no consistent relationship between the presence of antidromic action potentials and the presence of inhibition in response to stimulation of different sites. In addition, there was no correlation between antidromic and inhibitory response latencies. These results provide no clear support for the feedback model of inhibition. By contrast, there was a highly significant correlation between the latency of principal cell EPSPs and IPSPs, in support of a feedforward model of inhibition. Response latencies of candidate inhibitory neurons were also consistent with the feedforward model. The results provide evidence that an excitatory relay function of the entorhinal cortex and subicular complex is modified temporally by local, extrinsically activated inhibitory circuits.

[1]  E. Kandel,et al.  Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. , 1961, Journal of neurophysiology.

[2]  E. Kandel,et al.  Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons , 1961 .

[3]  William Mendenhall,et al.  Introduction to Probability and Statistics , 1961, The Mathematical Gazette.

[4]  D. Kerr,et al.  Collateral projection of the lateral olfactory tract to entorhinal cortical areas in the cat. , 1972, Brain research.

[5]  M. T. Shipley,et al.  Presubiculum afferents to the entorhinal area and the Papez circuit. , 1974, Brain research.

[6]  P. Andersen.  Organization of Hippocampal Neurons and Their Interconnections , 1975 .

[7]  T. Babb,et al.  Response decrement in a hippocampal basket cell , 1977, Brain Research.

[8]  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.

[9]  W. Levy,et al.  Anatomical evidence for interlamellar inhibition in the fascia dentata , 1978, Brain Research.

[10]  P. Schwartzkroin,et al.  Physiological and morphological identification of a nonpyramidal hippocampal cell type , 1978, Brain Research.

[11]  R. M. Beckstead.  Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell-labeling with horseradish peroxidase , 1978, Brain Research.

[12]  T. Babb,et al.  Neurophysiology of the caudally directed hippocampal efferent system in the rat: Projections to the subicular complex , 1980, Brain Research.

[13]  T. Babb,et al.  Inhibition in subicular and entorhinal principal neurons in response to electrical stimulation of the fornix and hippocampus , 1980, Brain Research.

[14]  P. Schwartzkroin,et al.  Local circuit synaptic interactions in hippocampal brain slices , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  G. Buzsáki,et al.  Direct afferent excitation and long-term potentiation of hippocampal interneurons. , 1982, Journal of neurophysiology.

[16]  R. Nicoll,et al.  Feed‐forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro , 1982, The Journal of physiology.

[17]  A. Alonso,et al.  Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain , 1982, Neuroscience Letters.

[18]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

[19]  F. Wouterlood,et al.  Terminations of olfactory afferents on layer II and III neurons in the entorhinal area: Degeneration-golgi-electron microscopic study in the rat , 1983, Neuroscience Letters.

[20]  T. Babb,et al.  Demonstration of axonal projections of neurons in the rat hippocampus and subiculum by intracellular injection of HRP , 1983, Brain Research.

[21]  A. Alonso,et al.  A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain , 1984, The Journal of comparative neurology.

[22]  Howard V. Wheal,et al.  In vivo and in vitro studies on putative interneurones in the rat hippocampus: Possible mediators of feed-forward inhibition , 1984, Brain Research.

[23]  J M Bower,et al.  Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. , 1984, Journal of neurophysiology.

[24]  A possible postsynaptic inhibitory action for GABAB receptors on hippocampal pyramidal cells , 1984, Neuropharmacology.

[25]  G. Buzsáki.  Feed-forward inhibition in the hippocampal formation , 1984, Progress in Neurobiology.

[26]  C. Ribak,et al.  Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feed-forward inhibition , 1984, Journal of neurocytology.

[27]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[28]  Intradendritic recordings from neurons of motor cortex of cats. , 1984, Journal of neurophysiology.

[29]  R K Wong,et al.  Unitary inhibitory synaptic potentials in the guinea‐pig hippocampus in vitro. , 1984, The Journal of physiology.

[30]  C. Köhler.  A projection from the deep layers of the entorhinal area to the hippocampal formation in the rat brain , 1985, Neuroscience Letters.

[31]  C. Ribak,et al.  A combined Golgi-electron microscopic study of non-pyramidal neurons in the CA 1 area of the hippocampus , 1985, Journal of neurocytology.

[32]  E. Mugnaini,et al.  Projection of olfactory bulb efferents to layer I GABAergic neurons in the entorhinal area. Combination of anterograde degeneration and immunoelectron microscopy in rat , 1985, Brain Research.

[33]  D. Finch,et al.  Neurophysiology of limbic system pathways in the rat: Projections from the amygdala to the entorhinal cortex , 1986, Brain Research.

[34]  R. North,et al.  Acetylcholine hyperpolarizes central neurones by acting on an M2 muscarinic receptor , 1986, Nature.

[35]  E. Buhl,et al.  Various types of non-pyramidal hippocampal neurons project to the septum and contralateral hippocampus , 1986, Brain Research.

[36]  A. Colino,et al.  Inhibitory response in enterhinal and subicular cortices after electrical stimulation of the lateral and basolateral amygdala of the rat , 1986, Brain Research.

[37]  B W Connors,et al.  Cellular physiology of the turtle visual cortex: synaptic properties and intrinsic circuitry , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. Lacaille,et al.  Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.