Newly learned auditory responses mediated by NMDA receptors in the owl inferior colliculus

Science

Volumn 271, Issue 5248, 1996, Pages 525-528

  Feldman, Daniel E ^a   Brainard, Michael S ^a   Knudsen, Eric I ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL TISSUE; ARTICLE; AUDITORY RESPONSE; BIRD; CONDITIONING; INFERIOR COLLICULUS; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL;

ANIMALIA; AVES; STRIGIFORMES; TYTO ALBA;

EID: 0030046108     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.271.5248.525     Document Type: Article

References (45)

1. M. F. Bear, A. Kleinschmidt, Q. Gu, W. Singer, J. Neurosci. 10, 909 (1990), H. T Cline, E A Debski, M. Constantine-Paton, Proc. Natl Acad. Sci. U.S.A. 84, 4342 (1987); W J. Scherer and S. B. Udin, J. Neurosci 9, 3837 (1989); J. T Schmidt, ibid. 10, 233 (1990).
2. M. F. Bear, A. Kleinschmidt, Q. Gu, W. Singer, J. Neurosci. 10, 909 (1990), H. T Cline, E A Debski, M. Constantine-Paton, Proc. Natl Acad. Sci. U.S.A. 84, 4342 (1987); W J. Scherer and S. B. Udin, J. Neurosci 9, 3837 (1989); J. T Schmidt, ibid. 10, 233 (1990).
3. M. F. Bear, A. Kleinschmidt, Q. Gu, W. Singer, J. Neurosci. 10, 909 (1990), H. T Cline, E A Debski, M. Constantine-Paton, Proc. Natl Acad. Sci. U.S.A. 84, 4342 (1987); W J. Scherer and S. B. Udin, J. Neurosci 9, 3837 (1989); J. T Schmidt, ibid. 10, 233 (1990).
4. M. F. Bear, A. Kleinschmidt, Q. Gu, W. Singer, J. Neurosci. 10, 909 (1990), H. T Cline, E A Debski, M. Constantine-Paton, Proc. Natl Acad. Sci. U.S.A. 84, 4342 (1987); W J. Scherer and S. B. Udin, J. Neurosci 9, 3837 (1989); J. T Schmidt, ibid. 10, 233 (1990).
5. N W. Daw, P. S. G Stein, K. Fox, Annu Rev. Neurosci. 16, 207 (1993); Y H. Kwon, M. Esguerra, M. Sur, J. Neurophysiol. 66, 414 (1991), K. Fox, H. Sato, N. Daw, J Neurosci. 9, 2443 (1989), K. D. Miller, B Chapman, M. P. Stryker, Proc. Natl Acad. Sci. U.S.A. 86, 5183 (1989)
6. N W. Daw, P. S. G Stein, K. Fox, Annu Rev. Neurosci. 16, 207 (1993); Y H. Kwon, M. Esguerra, M. Sur, J. Neurophysiol. 66, 414 (1991), K. Fox, H. Sato, N. Daw, J Neurosci. 9, 2443 (1989), K. D. Miller, B Chapman, M. P. Stryker, Proc. Natl Acad. Sci. U.S.A. 86, 5183 (1989)
7. N W. Daw, P. S. G Stein, K. Fox, Annu Rev. Neurosci. 16, 207 (1993); Y H. Kwon, M. Esguerra, M. Sur, J. Neurophysiol. 66, 414 (1991), K. Fox, H. Sato, N. Daw, J Neurosci. 9, 2443 (1989), K. D. Miller, B Chapman, M. P. Stryker, Proc. Natl Acad. Sci. U.S.A. 86, 5183 (1989)
8. N W. Daw, P. S. G Stein, K. Fox, Annu Rev. Neurosci. 16, 207 (1993); Y H. Kwon, M. Esguerra, M. Sur, J. Neurophysiol. 66, 414 (1991), K. Fox, H. Sato, N. Daw, J Neurosci. 9, 2443 (1989), K. D. Miller, B Chapman, M. P. Stryker, Proc. Natl Acad. Sci. U.S.A. 86, 5183 (1989)
9. Some of these results have been presented briefly elsewhere [M. S. Brainard and E. I. Knudsen, in Memory Concepts-1993, P. Andersen, O. Hvalby, O. Paulsen, B Hokfelt, Eds. (Elsevier, Amsterdam, Netherlands, 1993), pp. 113-125].
10. E I Knudsen, J Neurosci. 2, 1177 (1982); E. I. Knudsen, S. D. Esterly, S. duLac, ibid. 11, 1727 (1991), J F. Olsen, E. I. Knudsen, S. D. Esterly, ibid. 9, 2591 (1989).
11. E I Knudsen, J Neurosci. 2, 1177 (1982); E. I. Knudsen, S. D. Esterly, S. duLac, ibid. 11, 1727 (1991), J F. Olsen, E. I. Knudsen, S. D. Esterly, ibid. 9, 2591 (1989).
12. E I Knudsen, J Neurosci. 2, 1177 (1982); E. I. Knudsen, S. D. Esterly, S. duLac, ibid. 11, 1727 (1991), J F. Olsen, E. I. Knudsen, S. D. Esterly, ibid. 9, 2591 (1989).
13. E. I Knudsen and M S. Brainard, Science 253, 85 (1991).
14. M. S. Brainard and E. I. Knudsen, J. Neurosci. 13, 4589 (1993).
15. _, J Neurophysiol. 73, 595 (1995)
16. For each tectal site, we measured the VRF with prisms off and calculated the normal ITD tuning peak in microseconds as (2.5 × VRF azimuth in degrees) -2.7, from (6) The range of normal responses was defined as responses to ITDs within ±15 μs of this value. The range of learned responses was defined as responses to ITDs 40 ±15 μs displaced from the normal ITD value or, for double-peaked tuning curves, as responses to ITDs within ±15 μs of the abnormal response peak
17. D E Feldman and E I. Knudsen, J Neurosci 14, 5939 (1994)
18. N. P. Franks and W. R. Lieb, Nature 367, 607 (1994).
19. Ketamine injections reduced responses of ICX neurons to iontophoresed NMDA but not to the non-NMDA receptor agonist quisqualate. Responses to iontophoresed NMDA returned to control levels ≈50 mm after ketamine injection. Learned responses at transition state sites in prism-reared owls showed recovery that followed a similar time course
20. o laterally displacing prismatic spectacles. Prism-rearing, dichotic stimuli, and recording procedures were as in (6), and iontophoresis electrodes and solutions were as in (9) Owls were unanesthetized during data collection except for ketamine injections used to assess tuning changes
21. The effects of ketamine, AP-5, CNQX, and KYN on transition state ITD tuning curves were independent of the direction of prismatic displacement (right or left), the location of the normal VRF within frontal space, and the laterality of the recording site.
22. The ICX projects topographically to the tectum in normal owls [E. I. Knudsen and P. F Knudsen, J. Comp. Neurol. 218, 187 (1983)], and the topography is unchanged in prism-reared owls [D. E. Feldman and E. I. Knudsen, unpublished results). In prism-reared owls, transition state ITD tuning develops in the lateral portion of the ICX while the medial portion retains largely normal tuning. Therefore, an ICX site was considered topographically matched to a tectal site if it was located in the medial ICX and was tuned to an ITD matched within 15 μs to the normal ITD of the tectal site, or if tt was located in the lateral ICX and had ITD tuning that matched the tectal transition state tuning.
23. The ICX projects topographically to the tectum in normal owls [E. I. Knudsen and P. F Knudsen, J. Comp. Neurol. 218, 187 (1983)], and the topography is unchanged in prism-reared owls [D. E. Feldman and E. I. Knudsen, unpublished results). In prism-reared owls, transition state ITD tuning develops in the lateral portion of the ICX while the medial portion retains largely normal tuning. Therefore, an ICX site was considered topographically matched to a tectal site if it was located in the medial ICX and was tuned to an ITD matched within 15 μs to the normal ITD of the tectal site, or if tt was located in the lateral ICX and had ITD tuning that matched the tectal transition state tuning.
24. ITD tuning curves in Figs. 2 and 3 are means ± SEM of all curves collected during all control and recovery periods or during all drug application periods. On average, responses declined only 3% between the first and last control periods. Drug ejection was verified by observation of local blockade of auditory responses at each iCX iontophoresis site Drug iontophoresis significantly reduced tectal auditory responses at all sites reported in this study (26).
25. D E. Feldman, M. S Brainard, E I. Knudsen, data not shown.
26. The 80-nA current level for AP-5 and CNQX was chosen because it produced maximal tectal response blockade in both normal owls (79 ± 10% reduction of control responses, n = 17 sites) and prism-reared owls (82 ± 11% reduction, n = 5 transition state sites).
27. These properties are the hydrophobicity of CNQX and the relatively high concentration of KYN required for receptor blockade [G. L Collingridge and R A. J. Lester, Pharmacol Rev. 40, 143 (1989)]
28. Positional differences between ICX synapses mediating learned and normal responses cannot explain these results. If synapses mediating learned responses were located farther from the iontophoresis site than were pharmacologically identical synapses mediating normal responses, then all drugs, including AP-5, should block normal responses preferentially. Conversely, if synapses mediating learned responses were located nearer the iontophoresis site, then CNQX and KYN should preferentially block these responses, but they do not.
29. At many sites (Rg. 3D), CNQX blocked normal and learned responses equally. This may reflect a direct blockade of non-NMDA receptors together with an indirect reduction of NMDA receptor currents due to the voltage dependence of this receptor class [R A. Nicoll, R. C. Malenka, J. A Kauer, Physiol. Rev. 70, 513 (1990)].
30. J. J. O'Connor, M J. Rowan, R Anwyl, Nature 367, 557 (1994); G. Kohr, Y. D DeKoninck, I. Mody, J Neurosci. 13, 3612 (1993); H Gozlan, D. Diabira, P Chinestra, Y Ben-Ari, J. Neurophysiol 72, 3017 (1994).
31. J. J. O'Connor, M J. Rowan, R Anwyl, Nature 367, 557 (1994); G. Kohr, Y. D DeKoninck, I. Mody, J Neurosci. 13, 3612 (1993); H Gozlan, D. Diabira, P Chinestra, Y Ben-Ari, J. Neurophysiol 72, 3017 (1994).
32. J. J. O'Connor, M J. Rowan, R Anwyl, Nature 367, 557 (1994); G. Kohr, Y. D DeKoninck, I. Mody, J Neurosci. 13, 3612 (1993); H Gozlan, D. Diabira, P Chinestra, Y Ben-Ari, J. Neurophysiol 72, 3017 (1994).
33. It would be interesting to know whether the two pharmacologically distinct types of synapses were located on the same ICX neurons, as has been observed for single neurons in other systems [K. T. Sillar and A. Roberts, Brain Res 545, 24 (1991); R Mooney, J. Neurosci. 12, 2464 (1992); A. M. Thomson and J. Deuchars, Trends Neurosci. 17, 119 (1994)]. This issue cannot be resolved by extracellular recording, however, because even single ICX units that respond to both normal and teamed ITDs may receive inputs (via pharmacologically homogeneous synapses) from two different populations of ICX neurons, each of which expresses only a single subtype of EAA receptor.
34. It would be interesting to know whether the two pharmacologically distinct types of synapses were located on the same ICX neurons, as has been observed for single neurons in other systems [K. T. Sillar and A. Roberts, Brain Res 545, 24 (1991); R Mooney, J. Neurosci. 12, 2464 (1992); A. M. Thomson and J. Deuchars, Trends Neurosci. 17, 119 (1994)]. This issue cannot be resolved by extracellular recording, however, because even single ICX units that respond to both normal and teamed ITDs may receive inputs (via pharmacologically homogeneous synapses) from two different populations of ICX neurons, each of which expresses only a single subtype of EAA receptor.
35. It would be interesting to know whether the two pharmacologically distinct types of synapses were located on the same ICX neurons, as has been observed for single neurons in other systems [K. T. Sillar and A. Roberts, Brain Res 545, 24 (1991); R Mooney, J. Neurosci. 12, 2464 (1992); A. M. Thomson and J. Deuchars, Trends Neurosci. 17, 119 (1994)]. This issue cannot be resolved by extracellular recording, however, because even single ICX units that respond to both normal and teamed ITDs may receive inputs (via pharmacologically homogeneous synapses) from two different populations of ICX neurons, each of which expresses only a single subtype of EAA receptor.
36. E Aizenman, S A. Lipton, R H. Loring, Neuron 2, 1257 (1989); D. D. Molt and D. V. Lewis, Science 252, 1718 (1991), C. H. Davies, S. J. Starkley, M F Pozza, G. L Collingridge, Nature 349,609 (1991 ); Y. T. Wang and M. W Salter, ibid 369, 233 (1994).
37. E Aizenman, S A. Lipton, R H. Loring, Neuron 2, 1257 (1989); D. D. Molt and D. V. Lewis, Science 252, 1718 (1991), C. H. Davies, S. J. Starkley, M F Pozza, G. L Collingridge, Nature 349,609 (1991 ); Y. T. Wang and M. W Salter, ibid 369, 233 (1994).
38. E Aizenman, S A. Lipton, R H. Loring, Neuron 2, 1257 (1989); D. D. Molt and D. V. Lewis, Science 252, 1718 (1991), C. H. Davies, S. J. Starkley, M F Pozza, G. L Collingridge, Nature 349,609 (1991 ); Y. T. Wang and M. W Salter, ibid 369, 233 (1994).
39. E Aizenman, S A. Lipton, R H. Loring, Neuron 2, 1257 (1989); D. D. Molt and D. V. Lewis, Science 252, 1718 (1991), C. H. Davies, S. J. Starkley, M F Pozza, G. L Collingridge, Nature 349,609 (1991 ); Y. T. Wang and M. W Salter, ibid 369, 233 (1994).
40. D. Liao, N. A. Hessler, R. Malinow, Nature 375, 400 (1995), J. T Isaac, R. A. Nicoll, R. C. Malenka, Neuron 15, 427 (1995).
41. D. Liao, N. A. Hessler, R. Malinow, Nature 375, 400 (1995), J. T Isaac, R. A. Nicoll, R. C. Malenka, Neuron 15, 427 (1995).
42. D. V. Madison, R C Malenka, R A. Nicoll, Annu Rev. Neurosci. 14, 379 (1991).
43. We determined the significance of the drug effect (P < 0.05) by comparing all ITD tuning curves obtained during control/recovery and drug application periods by means of polynomial extension of the general linear test [R. Dunia and P. M. Narins, Hearing Res. 37, 241 (1989); J Neter W Wasserman, M H. Kutner. Applied Linear Statistical Models (Irwin, Homewood, IL. ed. 3, 1990)].
44. We determined the significance of the drug effect (P < 0.05) by comparing all ITD tuning curves obtained during control/recovery and drug application periods by means of polynomial extension of the general linear test [R. Dunia and P. M. Narins, Hearing Res. 37, 241 (1989); J Neter W Wasserman, M H. Kutner. Applied Linear Statistical Models (Irwin, Homewood, IL. ed. 3, 1990)].
45. Supported by NIH R01 DC00155-14 and by a Howard Hughes Medical institute Predoctoral Fellowship to D E F We thank Y Cohen for advice on the statistics.