Statistical properties of neuronal spike trains in the substantia nigra: Cell types and their interactions

Summary Spike trains from spontaneously active neurons in the substantia nigra of locally anesthetized, immobilized rats could be included in one of three broad categories, on the basis of the form of their autocorrelation histograms and spike waveforms. Initial brief trough (IBT) cells show a tendency not to fire for 10–50 msec after generation of an action potential. The duration of this period, which is seen as an initial trough in the auto-correlation histogram, is inversely related to firing rate for these neurons. Cells of this type fire repetitively at rates above 15–20/sec, and are found predominantly in the pars reticulata of the substantia nigra. Initial prolonged trough (IPT) cells have substantially longer initial troughs (60–250 msec) in their auto-correlation histograms, from which firing probability recovers more gradually. IPT cells have a trough length which increases with increasing firing rate for rates below 3–6/sec, the threshold for repetitive firing. They are found in the pars compacta and probably represent the dopaminergic neurons of that area. Bursty cells are much less numerous than cells of the other types, and are found in both parts of the substantia nigra, although about twice as commonly in pars reticulata. They fire in bursts of variable length, and may represent nigral interneurons. Cross-correlations between these different cell types suggest several potential synaptic interactions between neurons intrinsic to the substantia nigra. In addition, the possibility of shared excitatory or inhibitory input to different classes of neurons in the substantia nigra is discussed, as well as the relation of these statistical properties to neuropharmacological and anatomical observations on neurons of the substantia nigra.

[1]  D. Purpura,et al.  Electrophysiological analysis of reciprocal caudato-nigral relations. , 1967, Brain research.

[2]  H. L. Bryant,et al.  Correlations of neuronal spike discharges produced by monosynaptic connections and by common inputs. , 1973, Journal of neurophysiology.

[3]  R. MacGregor,et al.  Intrinsic oscillations in neural networks: A linear model for the nth-order loop , 1971 .

[4]  J. Kebabian,et al.  Dopamine-sensitive adenylate cyclase occurs in a region of substantia nigra containing dopaminergic dendrites. , 1976, Science.

[5]  J. Korf,et al.  Dopamine release in substantia nigra? , 1976, Nature.

[6]  U. Ungerstedt Stereotaxic mapping of the monoamine pathways in the rat brain. , 1971, Acta physiologica Scandinavica. Supplementum.

[7]  E. Rinvik Demonstration of nigrothalamic connections in the cat by retrograde axonal transport of horseradish peroxidase , 1975, Brain Research.

[8]  L. D. Harmon Neuromimes: Action of a Reciprocally Inhibitory Pair , 1964, Science.

[9]  U. Ungerstedt,et al.  On the distribution and possible function of monamine nerve terminals in the olfactory bulb of the rabbit. , 1965, Life sciences.

[10]  A. Björklund,et al.  Mesencephalic dopamine neurons projecting to neocortex. , 1974, Brain research.

[11]  D. Straughan,et al.  Synaptic mechanisms in the substantia nigra , 1976, The Journal of pharmacy and pharmacology.

[12]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[13]  B. Bunney,et al.  CENTRAL DOPAMINERGIC NEURONS: NEUROPHYSIOLOGICAL IDENTIFICATION AND RESPONSES TO DRUGS* , 1973 .

[14]  P. Groves,et al.  The substantia nigra of the rat: A golgi study , 1977, The Journal of comparative neurology.

[15]  T. Hökfelt,et al.  Histochemical support for a dopaminergic mechanism in the dendrites of certain periglomerular cells in the rat olfactory bulb , 1975, Neuroscience Letters.

[16]  P. Groves,et al.  Statistical properties of neurons in the rat mesencephalic reticular formation. , 1973, Brain research.

[17]  A L Towe,et al.  Extracellular microelectrode sampling bias. , 1970, Experimental neurology.

[18]  J. Eccles,et al.  Electrophysiological investigations on Renshaw cells , 1961, The Journal of physiology.

[19]  R. Gulley,et al.  The fine structure of the neurons in the rat substantia nigra. , 1971, Tissue & cell.

[20]  K. Fuxe,et al.  DEMONSTRATION AND MAPPING OUT OF NIGRO-NEOSTRIATAL DOPAMINE NEURONS. , 1964, Life sciences.

[21]  O. Hornykiewicz Dopamine (3-hydroxytyramine) and brain function. , 1966, Pharmacological reviews.

[22]  O. Lindvall,et al.  Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals , 1975, Brain Research.

[23]  A. Dray,et al.  Caudate stimulation and substantia nigra activity in the rat. , 1976, The Journal of physiology.

[24]  W. Nauta,et al.  Projections of the lentiform nucleus in the monkey. , 1966, Brain research.

[25]  P. Groves,et al.  Apparent feedback from the caudate nucleus to the substantia nigra following amphetamine administration , 1975, Neuropharmacology.

[26]  P. Groves,et al.  Amphetamine-induced release of dopamine from the substantia nigra in vitro. , 1976, Life sciences.

[27]  P. Groves,et al.  Slow rhythms and correlations in spike trains from midbrain neurons , 1975, Experimental Neurology.

[28]  T. Jessell,et al.  Release of dopamine from dendrites in rat substantia nigra , 1976, Nature.

[29]  Schwyn Rc,et al.  The primate substantia nigra: a Golgi and electron microscopic study. , 1974 .

[30]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[31]  Gordon M. Shephero Physiological evidence for dendrodendritic synaptic interactions in the rabbit's olfactory glomerulus , 1971 .

[32]  W. Calvin Some simple spike separation techniques for simultaneously recorded neurons. , 1973, Electroencephalography and clinical neurophysiology.

[33]  T. Tsubokawa,et al.  Suppression of cell firing in the substantia nigra by caudate nucleus stimulation. , 1972, Experimental neurology.

[34]  W. Calvin Generation of spike trains in CNS neurons , 1975, Brain Research.

[35]  W H Calvin,et al.  Three modes of repetitive firing and the role of threshold time course between spikes. , 1974, Brain research.

[36]  P. Groves,et al.  Biochemistry and behavior: some central actions of amphetamine and antipsychotic drugs. , 1976, Annual review of psychology.

[37]  G. Somjen,et al.  Electrophysiological study of corticocaudate projections in cats. , 1976, Journal of neurobiology.

[38]  J A Hobson,et al.  Discharge patterns of cat pontine brain stem neurons during desynchronized sleep. , 1975, Journal of neurophysiology.

[39]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[40]  S. L. Liles Single-unit responses of caudate neurons to stimulation of frontal cortex, substantia nigra and entopeduncular nucleus in cats. , 1974, Journal of neurophysiology.

[41]  S J Young,et al.  Self-inhibition by dopaminergic neurons , 1975, Science.

[42]  K. Koketsu,et al.  Cholinergic and inhibitory synapses in a pathway from motor‐axon collaterals to motoneurones , 1954, The Journal of physiology.

[43]  G. P. Moore,et al.  Statistical analysis and functional interpretation of neuronal spike data. , 1966, Annual review of physiology.

[44]  W. R. Adey,et al.  Correlated firing of hippocampal neuron pairs in sleep and wakefulness. , 1969, Experimental neurology.

[45]  M B Carpenter,et al.  Nigrostriatal and nigrothalamic fibers in the rhesus monkey , 1972, The Journal of comparative neurology.

[46]  O. Lindvall,et al.  The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. , 1974, Acta physiologica Scandinavica. Supplementum.

[47]  R. Roth,et al.  Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. , 1973, The Journal of pharmacology and experimental therapeutics.

[48]  W. Precht,et al.  Monosynaptic inhibition of neurons of the substantia nigra by caudato-nigral fibers. , 1971, Brain research.

[49]  R. Faull,et al.  Ascending projections of the substantia nigra in the rat , , 1968, The Journal of comparative neurology.

[50]  G. Gerstein,et al.  Interactions between cat lateral geniculate neurons. , 1976, Journal of neurophysiology.

[51]  K. Fuxe,et al.  EVIDENCE FOR THE EXISTENCE OF MONOAMINE-CONTAINING NEURONS IN THE CENTRAL NERVOUS SYSTEM. I. DEMONSTRATION OF MONOAMINES IN THE CELL BODIES OF BRAIN STEM NEURONS. , 1964, Acta physiologica Scandinavica. Supplementum.

[52]  J. Szabo,et al.  Topical distribution of the striatal efferents in the monkey , 1962 .