Local circuit interactions in synchronization of cortical neurones.

Under certain circumstances large numbers of neurones in the mammalian central nervous system (CNS) can discharge simultaneously. An example of such activity is recorded from a hippocampal slice in the presence of agents which block synaptic inhibition. This synchronized discharge occurs spontaneously in a rhythmic fashion or may be triggered by stimulation of any afferent pathway. Its generation appears to involve local circuit interactions. The favourable conditions offered by an in vitro preparation have allowed the cellular events during this activity to be examined in some detail. Three factors appear to be critically involved in the synchronization process. Firstly, the intrinsic ability of neurones to generate bursts, secondly, the existence of powerful recurrent excitatory connections, and thirdly the absence of inhibition which normally prevents the spread of bursting activity through the recurrent connections. Computer simulations show that in a sparsely connected network of bursting neurones activity initiated in a few cells may spread through recurrent connections until eventually the whole population discharges simultaneously. Rhythmic discharges similar to those described here also underly various CNS functions including centrally-originating motor patterns. It remains to be determined whether neuronal properties and connectivity found to be important in this hippocampal rhythm may also play a role in the generation of other rhythmic activities in the mammalian CNS.

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

[2]  D. Prince,et al.  Intradendritic recordings from hippocampal neurons. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. A. Marsan,et al.  CORTICAL CELLULAR PHENOMENA IN EXPERIMENTAL EPILEPSY: INTERICTAL MANIFESTATIONS. , 1964, Experimental neurology.

[4]  D. A. Brown,et al.  Calcium‐activated outward current in voltage‐clamped hippocampal neurones of the guinea‐pig. , 1983, The Journal of physiology.

[5]  R. Nicoll,et al.  Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells , 1984, Nature.

[6]  D. Prince,et al.  Participation of calcium spikes during intrinsic burst firing in hippocampal neurons , 1978, Brain Research.

[7]  R. Traub,et al.  Cellular mechanism of neuronal synchronization in epilepsy. , 1982, Science.

[8]  R K Wong,et al.  Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. , 1983, Journal of neurophysiology.

[9]  R K Wong,et al.  Afterpotential generation in hippocampal pyramidal cells. , 1981, Journal of neurophysiology.

[10]  D. Prince,et al.  Penicillin‐induced epileptiform activity in the hippocampal in vitro preparation , 1977, Annals of neurology.

[11]  R. Miles,et al.  Single neurones can initiate synchronized population discharge in the hippocampus , 1983, Nature.

[12]  Wong Rk,et al.  Synchronized burst discharge in disinhibited hippocampal slice. II. Model of cellular mechanism. , 1983 .

[13]  S. Andersson,et al.  Physiological basis of the alpha rhythm , 1968 .

[14]  R. Nicoll,et al.  Epileptiform burst afterhyperolarization: calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. , 1980, Science.

[15]  D. Prince,et al.  Cellular and field potential properties of epileptogenic hippocampal slices , 1978, Brain Research.

[16]  R. Wyman Neural generation of the breathing rhythm. , 1977, Annual review of physiology.

[17]  W. Spencer,et al.  Penicillin-induced interictal discharges from the cat hippocampus. I. Characteristics and topographical features. , 1969, Journal of neurophysiology.

[18]  P. Schwartzkroin,et al.  Effects of EGTA on the calcium-activated afterhyperpolarization in hippocampal CA3 pyramidal cells. , 1980, Science.

[19]  S. Grillner Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[20]  F. Edward Dudek,et al.  Local synaptic circuits in rat hippocampus: interactions between pyramidal cells , 1980, Brain Research.

[21]  R. Dingledine,et al.  Reduced inhibition during epileptiform activity in the in vitro hippocampal slice. , 1980, The Journal of physiology.

[22]  D. Prince,et al.  A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. , 1980, Journal of neurophysiology.

[23]  T. H. Brown,et al.  Giant synaptic potential hypothesis for epileptiform activity. , 1981, Science.

[24]  R. D. Traub,et al.  Synchronized afterdischarges in the hippocampus: Contribution of local synaptic interactions , 1984, Neuroscience.

[25]  R K Wong,et al.  Dendritic mechanisms underlying penicillin-induced epileptiform activity. , 1979, Science.

[26]  B. Alger Characteristics of a slow hyperpolarizing synaptic potential in rat hippocampal pyramidal cells in vitro. , 1984, Journal of neurophysiology.

[27]  D. Johnston,et al.  Voltage clamp discloses slow inward current in hippocampal burst-firing neurones , 1980, Nature.

[28]  D. A. Brown,et al.  Persistent slow inward calcium current in voltage‐clamped hippocampal neurones of the guinea‐pig. , 1983, The Journal of physiology.

[29]  W. Spencer,et al.  Recurrent excitation in the CA3 region of cat hippocampus. , 1971, The International journal of neuroscience.

[30]  J. Eccles,et al.  Hippocampus of the Brain: Recurrent Inhibition in the Hippocampus with Identification of the Inhibitory Cell and its Synapses , 1963, Nature.

[31]  Y Fujita,et al.  INTRACELLULAR RECORDS FROM HIPPOCAMPAL PYRAMIDAL CELLS IN RABBIT DURING THETA RHYTHM ACTIVITY. , 1964, Journal of neurophysiology.

[32]  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.

[33]  E. Kandel,et al.  Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. , 1961, Journal of neurophysiology.

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