Thalamic Relay of Spontaneous Retinal Activity Prior to Vision

Before vision, retinal ganglion cells produce spontaneous waves of action potentials. A crucial question is whether this spontaneous activity is transmitted to lateral geniculate nucleus (LGN) neurons. Using a novel in vitro preparation, we report that LGN neurons receive periodic barrages of postsynaptic currents from the retina that drive them to fire bursts of action potentials. Groups of LGN neurons are highly correlated in their firing. Experiments in wild-type and NMDAR1 knockout mice show that NMDA receptor activation is not necessary for firing. The transmission of the highly correlated retinal activity to the LGN supports the hypothesis that retinal waves drive retinogeniculate synaptic remodeling. Because LGN neurons are driven to fire action potentials, this spontaneous activity could also act more centrally to influence synaptic modification within the developing visual cortex.

[1]  D. McCormick,et al.  Postnatal development of synchronized network oscillations in the ferret dorsal lateral geniculate and perigeniculate nuclei , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  M. Sur,et al.  An N-methyl-D-aspartate receptor antagonist does not prevent eye-specific segregation in the ferret retinogeniculate pathway , 1994, Brain Research.

[3]  Damon L. McCormick,et al.  Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  C. Shatz Impulse activity and the patterning of connections during cns development , 1990, Neuron.

[5]  P. Rakic Prenatal genesis of connections subserving ocular dominance in the rhesus monkey , 1976, Nature.

[6]  S. Sherman,et al.  N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

[8]  C. Shatz,et al.  Transient period of correlated bursting activity during development of the mammalian retina , 1993, Neuron.

[9]  M. Bear,et al.  Mechanism for a sliding synaptic modification threshold , 1995, Neuron.

[10]  C. Mason Development of terminal arbors of retino-geniculate axons in the kitten—I. Light microscopical observations , 1982, Neuroscience.

[11]  D. Baylor,et al.  Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. , 1991, Science.

[12]  Susumu Tonegawa,et al.  Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice , 1994, Cell.

[13]  D. Hocking,et al.  An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[15]  C. Shatz,et al.  Prenatal development of functional connections in the cat's retinogeniculate pathway , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  C. Shatz,et al.  Early functional neural networks in the developing retina , 1995, Nature.

[17]  K D Miller,et al.  Models of activity-dependent neural development. , 1992, Progress in brain research.

[18]  E. W. Kairiss,et al.  Hebbian synapses: biophysical mechanisms and algorithms. , 1990, Annual review of neuroscience.

[19]  Richard Mooney,et al.  Enhancement of transmission at the developing retinogeniculate synapse , 1993, Neuron.

[20]  L. Maffei,et al.  Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[21]  M. Stryker,et al.  Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  F. Werblin,et al.  Requirement for Cholinergic Synaptic Transmission in the Propagation of Spontaneous Retinal Waves , 1996, Science.

[23]  M Imbert,et al.  Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse , 1984, The Journal of comparative neurology.

[24]  M. Bear,et al.  Synaptic plasticity: LTP and LTD , 1994, Current Opinion in Neurobiology.

[25]  M. Sur,et al.  Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors , 1991, Nature.

[26]  R. Linsker,et al.  From basic network principles to neural architecture , 1986 .

[27]  C. Shatz,et al.  Synapses formed by identified retinogeniculate axons during the segregation of eye input , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Sur,et al.  Retinogeniculate EPSPs recorded intracellularly in the ferret lateral geniculate nucleus in vitro: Role of NMDA receptors , 1992, Visual Neuroscience.

[29]  C. Mason Development of terminal arbors of retino-geniculate axons in the kitten—II. Electron microscopical observations , 1982, Neuroscience.

[30]  C. Shatz,et al.  Developmental mechanisms that generate precise patterns of neuronal connectivity , 1993, Cell.

[31]  D. Linden,et al.  Long-term synaptic depression. , 1995, Annual review of neuroscience.

[32]  M. Dubin,et al.  Elimination of action potentials blocks the structural development of retinogeniculate synapses , 1986, Nature.

[33]  M. Pirchio,et al.  On the excitatory post‐synaptic potential evoked by stimulation of the optic tract in the rat lateral geniculate nucleus. , 1987, The Journal of physiology.

[34]  R. Nicoll,et al.  Contrasting properties of two forms of long-term potentiation in the hippocampus , 1995, Nature.

[35]  C. Blakemore,et al.  Innate and environmental factors in the development of the kitten's visual cortex. , 1975, The Journal of physiology.

[36]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[37]  D. Hubel,et al.  Ordered arrangement of orientation columns in monkeys lacking visual experience , 1974, The Journal of comparative neurology.

[38]  A. Levey,et al.  The origins of cholinergic and other subcortical afferents to the thalamus in the rat , 1987, The Journal of comparative neurology.

[39]  R Linsker,et al.  From basic network principles to neural architecture: emergence of orientation-selective cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Stryker,et al.  Development of orientation selectivity in ferret visual cortex and effects of deprivation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.