The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation

Electrical stimulation of the thalamus has been widely used to test for the existence of monosynaptic input to cortical neurons, typically with stimulation currents that evoke cortical spikes with high probability. We stimulated the lateral geniculate nucleus (LGN) of the thalamus and recorded monosynaptically evoked spikes from layer 4 neurons in visual cortex. We found that with moderate currents, cortical spikes were evoked with low to moderate probability and their occurrence was modulated by ongoing sensory (visual) input. Furthermore, when repeated at 8–12 Hz, electrical stimulation of the thalamic afferents caused such profound inhibition that cortical spiking activity was suppressed, aside from electrically evoked monosynaptic spikes. Visual input to layer 4 cortical cells between electrical stimuli must therefore have derived exclusively from LGN afferents. We used white-noise visual stimuli to make a 2D map of the receptive field of each cortical simple cell during repetitive electrical stimulation in the LGN. The receptive field of electrically evoked monosynaptic spikes (and thus of the thalamic input alone) was significantly elongated. Its primary subfield was comparable to that of the control receptive field, but secondary (flanking) subfields were weaker. These findings extend previous results from intracellular recordings, but also demonstrate the effectiveness of an extracellular method of measuring subthreshold afferent input to cortex.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  W. Precht The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[3]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[4]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[5]  D. Ferster,et al.  An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat. , 1983, The Journal of physiology.

[6]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[7]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  S. Sherman,et al.  Postsynaptic potentials recorded in neurons of the cat's lateral geniculate nucleus following electrical stimulation of the optic chiasm. , 1988, Journal of neurophysiology.

[9]  H. Swadlow Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. , 1988, Journal of neurophysiology.

[10]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[11]  D. Whitteridge,et al.  Mechanisms of inhibition in cat visual cortex. , 1991, The Journal of physiology.

[12]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[13]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[15]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[16]  C. Gray,et al.  Physiological properties of inhibitory interneurons in cat striate cortex. , 1997, Cerebral cortex.

[17]  R. Shapley,et al.  New perspectives on the mechanisms for orientation selectivity , 1997, Current Opinion in Neurobiology.

[18]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[19]  M. Sirota,et al.  Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. , 1998, Journal of neurophysiology.

[20]  D. Ferster,et al.  Strength and Orientation Tuning of the Thalamic Input to Simple Cells Revealed by Electrically Evoked Cortical Suppression , 1998, Neuron.

[21]  R. Reid,et al.  Low Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons , 2000, Neuron.

[22]  M. Carandini,et al.  Membrane Potential and Firing Rate in Cat Primary Visual Cortex , 2000, The Journal of Neuroscience.

[23]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[24]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

[25]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[26]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[27]  A. Grinvald,et al.  Dynamics and Constancy in Cortical Spatiotemporal Patterns of Orientation Processing , 2002, Science.