Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo

Science

Volumn 285, Issue 5427, 1999, Pages 599-604

  Weliky, Michael ^a,b   Katz, C ^b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BINOCULAR VISION; BRAIN MATURATION; FERRET; LATERAL GENICULATE BODY; NERVE CELL NETWORK; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; VISUAL STIMULATION; VISUAL SYSTEM;

ACTION POTENTIALS; ANIMALS; DENERVATION; ELECTRODES; FEEDBACK; FERRETS; GENICULATE BODIES; MODELS, NEUROLOGICAL; NEURONS; OPTIC NERVE; RETINA; RETINAL GANGLION CELLS; THALAMUS; VISUAL CORTEX; VISUAL PATHWAYS;

ANIMALIA; MUSTELA; MUSTELA PUTORIUS FURO;

EID: 0033597869     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5427.599     Document Type: Article

References (46)

1. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
2. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
3. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
4. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
5. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
6. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
7. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 978 (1963); ibid., p. 1003; D. H. Hubel and T. N. Wiesel, J. Physiol. 206, 419 (1970); _, S. LeVay, Philos. Trans. R. Soc. London Ser. B 278, 377 (1977); J. D. Pettigrew, J. Physiol. 237, 49 (1974); B. Chapman and M. P. Stryker, J. Neurosci. 13, 5251 (1993); M. C. Crair, E. S. Ruthazer, D. C. Gillespie, M. P. Stryker, Neuron 19, 307 (1997).
8. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 994 (1963); J. Comp. Neurol. 158, 307 (1974); P. Rakic, Philos. Trans. R. Soc. London Ser. B 278, 245 (1977); B. Chapman, M. P. Stryker, T. Bonhoeffer, J. Neurosci. 16, 6443 (1996).
9. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 994 (1963); J. Comp. Neurol. 158, 307 (1974); P. Rakic, Philos. Trans. R. Soc. London Ser. B 278, 245 (1977); B. Chapman, M. P. Stryker, T. Bonhoeffer, J. Neurosci. 16, 6443 (1996).
10. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 994 (1963); J. Comp. Neurol. 158, 307 (1974); P. Rakic, Philos. Trans. R. Soc. London Ser. B 278, 245 (1977); B. Chapman, M. P. Stryker, T. Bonhoeffer, J. Neurosci. 16, 6443 (1996).
11. T. N. Wiesel and D. H. Hubel, J. Neurophysiol. 26, 994 (1963); J. Comp. Neurol. 158, 307 (1974); P. Rakic, Philos. Trans. R. Soc. London Ser. B 278, 245 (1977); B. Chapman, M. P. Stryker, T. Bonhoeffer, J. Neurosci. 16, 6443 (1996).
12. M. C. Crair, D. C. Gillespie, M. P. Stryker, Science 279, 566 (1998).
13. J. C. Horton and D. R. Hocking, J. Neurosci. 16, 1791 (1996).
14. L. Maffei and L. Galli-Resta, Proc. Natl. Acad. Sci. U.S.A. 87, 2861 (1990); M. Meister, R. O. L. Wong, D. A. Baylor, C. J. Shatz, Science 252, 939 (1991); R. O. L. Wong, M. Meister, C. J. Shatz, Neuron 11, 923 (1993).
15. L. Maffei and L. Galli-Resta, Proc. Natl. Acad. Sci. U.S.A. 87, 2861 (1990); M. Meister, R. O. L. Wong, D. A. Baylor, C. J. Shatz, Science 252, 939 (1991); R. O. L. Wong, M. Meister, C. J. Shatz, Neuron 11, 923 (1993).
16. L. Maffei and L. Galli-Resta, Proc. Natl. Acad. Sci. U.S.A. 87, 2861 (1990); M. Meister, R. O. L. Wong, D. A. Baylor, C. J. Shatz, Science 252, 939 (1991); R. O. L. Wong, M. Meister, C. J. Shatz, Neuron 11, 923 (1993).
17. R. O. L. Wong and D. M. Oakley, Neuron 16, 1087 (1996).
18. B. Hu, M. Steriade, M. Beschenes, Neuroscience 31, 13 (1989); S. M. Lu, W. Guido, S. M. Sherman, Vis. Neurosci. 10, 631 (1993); P. C. Murphy, D. J. Uhlrich, N. Tamamaki, S. M. Sherman, ibid. 11, 781 (1994).
19. B. Hu, M. Steriade, M. Beschenes, Neuroscience 31, 13 (1989); S. M. Lu, W. Guido, S. M. Sherman, Vis. Neurosci. 10, 631 (1993); P. C. Murphy, D. J. Uhlrich, N. Tamamaki, S. M. Sherman, ibid. 11, 781 (1994).
20. B. Hu, M. Steriade, M. Beschenes, Neuroscience 31, 13 (1989); S. M. Lu, W. Guido, S. M. Sherman, Vis. Neurosci. 10, 631 (1993); P. C. Murphy, D. J. Uhlrich, N. Tamamaki, S. M. Sherman, ibid. 11, 781 (1994).
21. H. Hollander, Brain Res. 41, 464 (1972).
22. T. Bal, M. von Krosigk, D. A. McCormick, J. Physiol. 483, 665 (1995).
23. D. A. McCormick, F. Trent, A. S. Ramoa, J. Neurosci. 15, 5739 (1995).
24. The laminar identity of cells recorded by each electrode was determined by affixing small lights, housed within an opaque housing, in front of each eyelid, which were alternately flashed while recording evoked spike discharges. Typically, the microwire electrodes recorded large-amplitude multiunit or single-unit spike activity from one layer, together with smaller amplitude spike activity originating from an adjacent layer. For each electrode, amplitude discrimination techniques reliably isolated neuronal activity originating from the functional layer that produced the largest amplitude spikes. The functional identity of cells was assessed every 30 to 90 min with light flashes to each eye throughout the recording period. This assessment ensured that any slow shifts in recording positions that might recruit new cells from different functional layers would be identified (19). The cells identified during each light flash test session were used to discriminate spikes from subsequent spontaneous activity recordings until the next test session. Spike discrimination was accomplished with a custom LABVIEW program. Typically, each discrimination test session consisted of 8 to 15 light flash sequences, where each sequence consisted of one light flash to each eye (see Fig. 1B). The discrimination procedure was carried out independently at each electrode by first simultaneously displaying evoked spike trains from all light flash sequences from the test session on a computer display. Cursors could be moved up and down simultaneously on all spike train displays representing a single voltage threshold level. Spikes having an amplitude greater than this level were accepted by the program, and a poststimulus time histogram (PSTH) was constructed from all flash sequences and displayed. A spike amplitude threshold was established for each electrode by adjusting the voltage level until the PSTH showed that all accepted spikes were evoked by either light flash onset or offset to only one eye. These voltage levels were subsequently used to discriminate spikes from each electrode until the next discrimination test session.
25. Animals were anaesthetized with a mixture of ketamine hydrochloride [40 mg/kg intramuscularly (i.m.)] and xylazine hydrochloride (2 mg/kg i.m.) and placed in a stereotaxic holder. A 4 mm by 4 mm section of skull was removed and centered at 5 mm posterior to bregma and 5 mm lateral to the midline, and the exposed dura was reflected. The LGN surface was visually exposed by aspirating a 1-to 2-mm bore hole, centered within the region of exposed cortex, vertically through the brain with a small-diameter blunt syringe needle. A single recording electrode was used to first determine the location and size of the small region of ipsilaterally projecting retinal input with miniature light bulbs, placed in front of each eye, which were alternately flashed, and the response type of recorded neurons (that is, ON/OFF, ipsilatera(/contralateral eye) was assessed. The single recording electrode was removed, and the multielectrode array, attached to the headset, was lowered superficially (100 to 200 μm) into the LGN such that roughly half of the eight recording electrodes were within the region of ipsilaterally projecting retinal input. The bore hole was filled with agar to immobilize the LGN and surrounding tissue, and the headset was affixed to the skull with dental acrylic. The multielectrode array consisted of eight 12.5-μm diameter insulated tungsten wires (California Fine Wire, Grover Beach, CA) spaced 100 μm apart in a single row and cut to the same length. The electrodes were glued to a 1-mm-wide shaft of 50-μm-thick tungsten sheet, which was in turn affixed to small plate within the metal headset. The plate could be moved up and down by turning a 4 threads/mm screw, thereby raising or lowering all electrodes simultaneously. During recording, animals were free to move within a low-walled small plastic box placed on a heating blanket. All recordings of spontaneous activity were performed in a dark room. 0.45-m-long small-diameter low-noise coaxial cables connected the animal's headset to custom-made first-stage amplifiers providing 40,000 gain. Two-stage RC circuits bandpass filtered the signal between 600 and 6000 Hz. The amplifiers were mounted above the animal to provide freedom of movement within the box. The amplifiers output was fed into a PC plug-in A/D board (National Instruments, Austin, TX) and digitized at 10 kHz. The acquisition was controlled through custom software written in LABVIEW.
26. 2 describes the strength of the association between two variables. Values of r range from -1.0 to 1.0. Points in X represent binned spike counts (bin size ranging from 20 to 260 ms) at succesive time points (time interval equals the bin size) during a 100-s recording for one electrode. Points in Y represent the corresponding binned spike counts at a second electrode. This cross-correlation coefficient provides a normalized measurement of the covariance of spike firing rates independent of levels of neuronal activity.
27. At each electrode, binned spikes within each 100-s trial were shifted forward in time a random amount (from 0 to 100 s). Spikes that were shifted beyond the 100-s time point were wrapped around to time 0 + t. Correlation coefficients were calculated between shifted spike trains for all electrode pairs. For each 100-s trial, spike trains were shifted 100 times, and an average correlation coefficient was obtained for each electrode pair
28. The cross-correlation function between spike trains recorded at two electrodes was calculated by computing all time intervals between a spike at one electrode and a spike at the second electrode during a 100-s recording trial, binned into successive 2-ms time bins. The result was divided by the total number of spikes from the first electrode and the bin width. This yields a histogram of the spike firing rate at electrode 2 as a function of time since a spike from electrode 1. This result was normalized by dividing by the total number of spikes from the second electrode and multiplying it by a scale factor of 1000.
29. P. C. Murphy and A. M. Silito, J. Neurosci. 16, 1180 (1996).
30. Animals were anaesthetized by freely breathing a mixture of 2:1 nitrous oxide:oxygen, supplemented by 2.0 to 4.0% Halothane. The posterior region of occipital cortex, about 10 mm by 6 mm, was aspirated with a small-diameter blunt syringe needle. The resulting void was filled with sterile gel foam.
31. The connective tissue and muscles attaching the eyeball to the orbit were cut away. Fine scissors were used to reach behind the eyeball and cut the optic nerve. The rear portion of the eyeball was rotated into view to visually confirm optic nerve transection.
32. After transection of both optic nerves, the functional identity of cells recorded by each electrode could not be directly assessed with light flashes. However, in experiments in which only one optic nerve was cut, almost all electrodes recorded from the same functional layers driven by the intact eye both before and after the surgery, although shifts were occasionally observed at electrodes near layer boundaries. Furthermore, although slow gradual shifts between adjacent layers were also found to occur at electrodes over extended recording periods of 10 to 24 hours, electrodes typically recorded from the same eye-specific and ON/OFF layers. Therefore, we did not label the identity of units recorded after transection of both optic nerves (see Fig. 4, B and C); however, it is likely that most electrodes were still recording from the same LGN layers.
33. D. Contreras, A. Destexhe, T. J. Sejnowski, M. Steriade, Science 274, 771 (1996); D. A. Coulter and C. J. Lee, Brain Res. 631, 137 (1993); C. Q. Kao and D. A. Coulter, J. Neurophysiol. 77, 2661 (1997).
34. D. Contreras, A. Destexhe, T. J. Sejnowski, M. Steriade, Science 274, 771 (1996); D. A. Coulter and C. J. Lee, Brain Res. 631, 137 (1993); C. Q. Kao and D. A. Coulter, J. Neurophysiol. 77, 2661 (1997).
35. D. Contreras, A. Destexhe, T. J. Sejnowski, M. Steriade, Science 274, 771 (1996); D. A. Coulter and C. J. Lee, Brain Res. 631, 137 (1993); C. Q. Kao and D. A. Coulter, J. Neurophysiol. 77, 2661 (1997).
36. D. W. Godwin et al., J. Neurosci. 16, 8181 (1996).
37. F. S. Lo and S. M. Sherman, Exp. Brain Res. 100, 365 (1994).
38. U. Kim, M. V. Sanchez-Vives, D. A. McCormick, Science 27B, 130 (1997).
39. R. Mooney, A. A. Penn, R. Gallego, C. J. Shatz, Neuron 17, 863 (1996).
40. I. Godecke, D. S. Kim, T. Bonhoeffer, W. Singer, Eur. J. Neurosci. 9, 1754 (1997).
41. K. D. Miller, J. Neurosci. 14, 409 (1994).
42. E. Erwin and K. D. Miller, ibid. 18, 9870 (1998).
43. N. V. Swindale, Proc. R. Soc. London Ser. B Biol. Sci. 208, 243 (1980); K. D. Miller, J. B. Keller, M. P. Stryker, Science 245, 605 (1989).
44. N. V. Swindale, Proc. R. Soc. London Ser. B Biol. Sci. 208, 243 (1980); K. D. Miller, J. B. Keller, M. P. Stryker, Science 245, 605 (1989).
45. E. S. Ruthazer and M. P. Stryker, J. Neurosci. 16, 7253 (1996).
46. L.C.K. is an Investigator of the Howard Hughes Medical Institute. Also supported by grants from the NIH (National Eye Institute).