Cortical map reorganization enabled by nucleus basalis activity

Science

Volumn 279, Issue 5357, 1998, Pages 1714-1718

  Kilgard, Michael P ^a   Merzenich, Michael M ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN MAPPING; CONTROLLED STUDY; ELECTROSTIMULATION; FOREBRAIN; NONHUMAN; OLIVARY NUCLEUS; PLASTICITY; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; TRAINING;

ACETYLCHOLINE; ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; BASAL GANGLIA; BRAIN MAPPING; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; NEURONAL PLASTICITY; NEURONS; PROSENCEPHALON; RATS;

ANIMALIA;

EID: 0032513387     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5357.1714     Document Type: Article

References (46)

1. W. Singer. Eur. Arch. Psych. Neurol. Sci. 236, 4 (1986).
2. E. L. Thorndike, Animal Intelligence (Macmillan, New York, 1911).
3. E. Ahissar et al., Science 257, 1412 (1992); N. M. Weinberger, Curr. Opin. Neurobiol. 3, 570 (1993); E. Ahissar and M. Ahissar, ibid. 4, 80 (1994).
4. E. Ahissar et al., Science 257, 1412 (1992); N. M. Weinberger, Curr. Opin. Neurobiol. 3, 570 (1993); E. Ahissar and M. Ahissar, ibid. 4, 80 (1994).
5. E. Ahissar et al., Science 257, 1412 (1992); N. M. Weinberger, Curr. Opin. Neurobiol. 3, 570 (1993); E. Ahissar and M. Ahissar, ibid. 4, 80 (1994).
6. M. M. Merzenich, G. H. Recanzone, W. M. Jenkins, K. A. Grajski, Cold Spring Harbor Symp. Quant. Biol. 55, 873 (1990).
7. M. M. Mesulam, E. J. Mufson, B. H. Wainer, A. I. Levey, Neuroscience 10, 1185 (1983); D. B. Rye, B. H. Wainer, M. M. Mesulam, E. J. Mufson, C. B. Saper, ibid. 13, 627 (1984); M. Steriade and D. Biesold, Brain Cholinergic Systems (Oxford Univ. Press, New York, 1990).
8. M. M. Mesulam, E. J. Mufson, B. H. Wainer, A. I. Levey, Neuroscience 10, 1185 (1983); D. B. Rye, B. H. Wainer, M. M. Mesulam, E. J. Mufson, C. B. Saper, ibid. 13, 627 (1984); M. Steriade and D. Biesold, Brain Cholinergic Systems (Oxford Univ. Press, New York, 1990).
9. M. M. Mesulam, E. J. Mufson, B. H. Wainer, A. I. Levey, Neuroscience 10, 1185 (1983); D. B. Rye, B. H. Wainer, M. M. Mesulam, E. J. Mufson, C. B. Saper, ibid. 13, 627 (1984); M. Steriade and D. Biesold, Brain Cholinergic Systems (Oxford Univ. Press, New York, 1990).
10. R. T. Richardson and M. R. DeLong, in Activation to Acquisition. Functional Aspects of the Basal Forebrain Cholinergic System (Birkhauser, Boston, 1991), pp. 135-166; R. T. Richardson and M. R. DeLong, Adv. Exp. Med. Biol. 295, 233 (1991); A. E. Butt, G. Testylier, R. W. Dykes, Psychobiology 25, 18 (1997).
11. R. T. Richardson and M. R. DeLong, in Activation to Acquisition. Functional Aspects of the Basal Forebrain Cholinergic System (Birkhauser, Boston, 1991), pp. 135-166; R. T. Richardson and M. R. DeLong, Adv. Exp. Med. Biol. 295, 233 (1991); A. E. Butt, G. Testylier, R. W. Dykes, Psychobiology 25, 18 (1997).
12. R. T. Richardson and M. R. DeLong, in Activation to Acquisition. Functional Aspects of the Basal Forebrain Cholinergic System (Birkhauser, Boston, 1991), pp. 135-166; R. T. Richardson and M. R. DeLong, Adv. Exp. Med. Biol. 295, 233 (1991); A. E. Butt, G. Testylier, R. W. Dykes, Psychobiology 25, 18 (1997).
13. R. C. Peterson, Psychopharmacology 52, 283 (1977); H. H. Webster, U. Hanisch, R. W. Dykes, D. Biesold, Somatosens. Mot. Res. 8, 327 (1991); A. E. Butt and G. K. Hodge, Behav. Neurosci. 109, 699 (1995); G. Leanza et al., Eur. J. Neurosci. 8, 1535 (1996); K. A. Baskerville, J. B. Schweitzer, P. Herron, Neuroscience 80, 1159 (1997).
14. R. C. Peterson, Psychopharmacology 52, 283 (1977); H. H. Webster, U. Hanisch, R. W. Dykes, D. Biesold, Somatosens. Mot. Res. 8, 327 (1991); A. E. Butt and G. K. Hodge, Behav. Neurosci. 109, 699 (1995); G. Leanza et al., Eur. J. Neurosci. 8, 1535 (1996); K. A. Baskerville, J. B. Schweitzer, P. Herron, Neuroscience 80, 1159 (1997).
15. R. C. Peterson, Psychopharmacology 52, 283 (1977); H. H. Webster, U. Hanisch, R. W. Dykes, D. Biesold, Somatosens. Mot. Res. 8, 327 (1991); A. E. Butt and G. K. Hodge, Behav. Neurosci. 109, 699 (1995); G. Leanza et al., Eur. J. Neurosci. 8, 1535 (1996); K. A. Baskerville, J. B. Schweitzer, P. Herron, Neuroscience 80, 1159 (1997).
16. R. C. Peterson, Psychopharmacology 52, 283 (1977); H. H. Webster, U. Hanisch, R. W. Dykes, D. Biesold, Somatosens. Mot. Res. 8, 327 (1991); A. E. Butt and G. K. Hodge, Behav. Neurosci. 109, 699 (1995); G. Leanza et al., Eur. J. Neurosci. 8, 1535 (1996); K. A. Baskerville, J. B. Schweitzer, P. Herron, Neuroscience 80, 1159 (1997).
17. R. C. Peterson, Psychopharmacology 52, 283 (1977); H. H. Webster, U. Hanisch, R. W. Dykes, D. Biesold, Somatosens. Mot. Res. 8, 327 (1991); A. E. Butt and G. K. Hodge, Behav. Neurosci. 109, 699 (1995); G. Leanza et al., Eur. J. Neurosci. 8, 1535 (1996); K. A. Baskerville, J. B. Schweitzer, P. Herron, Neuroscience 80, 1159 (1997).
18. R. Metherate and J. H. Ashe, Brain Res. 559, 163 (1991); Synapse 14, 132 (1993); J. M. Edeline, C. Maho, B. Hars, E. Hennevin, Brain Res. 636, 333 (1994); J. M. Edeline, B. Hars, C. Maho, E. Hennevin, Exp. Brain Res. 97, 373 (1994).
19. R. Metherate and J. H. Ashe, Brain Res. 559, 163 (1991); Synapse 14, 132 (1993); J. M. Edeline, C. Maho, B. Hars, E. Hennevin, Brain Res. 636, 333 (1994); J. M. Edeline, B. Hars, C. Maho, E. Hennevin, Exp. Brain Res. 97, 373 (1994).
20. R. Metherate and J. H. Ashe, Brain Res. 559, 163 (1991); Synapse 14, 132 (1993); J. M. Edeline, C. Maho, B. Hars, E. Hennevin, Brain Res. 636, 333 (1994); J. M. Edeline, B. Hars, C. Maho, E. Hennevin, Exp. Brain Res. 97, 373 (1994).
21. R. Metherate and J. H. Ashe, Brain Res. 559, 163 (1991); Synapse 14, 132 (1993); J. M. Edeline, C. Maho, B. Hars, E. Hennevin, Brain Res. 636, 333 (1994); J. M. Edeline, B. Hars, C. Maho, E. Hennevin, Exp. Brain Res. 97, 373 (1994).
22. R. Metherate, N. Tremblay, R. W. Dykes, J. Neurophysiol. 59, 1231 (1988); T. M. McKenna, J. H. Ashe, N. M. Weinberger, Synapse 4, 30 (1989); R. Metherate and N. M. Weinberger, Brain Res. 480, 372 (1989); Synapse 6, 133 (1990).
23. R. Metherate, N. Tremblay, R. W. Dykes, J. Neurophysiol. 59, 1231 (1988); T. M. McKenna, J. H. Ashe, N. M. Weinberger, Synapse 4, 30 (1989); R. Metherate and N. M. Weinberger, Brain Res. 480, 372 (1989); Synapse 6, 133 (1990).
24. R. Metherate, N. Tremblay, R. W. Dykes, J. Neurophysiol. 59, 1231 (1988); T. M. McKenna, J. H. Ashe, N. M. Weinberger, Synapse 4, 30 (1989); R. Metherate and N. M. Weinberger, Brain Res. 480, 372 (1989); Synapse 6, 133 (1990).
25. R. Metherate, N. Tremblay, R. W. Dykes, J. Neurophysiol. 59, 1231 (1988); T. M. McKenna, J. H. Ashe, N. M. Weinberger, Synapse 4, 30 (1989); R. Metherate and N. M. Weinberger, Brain Res. 480, 372 (1989); Synapse 6, 133 (1990).
26. Although studies using stimulation of the NB reported mostly facilitation of the response to the paired stimulus, in several studies using local administration of ACh to alter receptive field organization the opposite effect was reported. In these studies, ACh most often caused a significant stimulus-specific decrease in cortical responsiveness after the pairing procedure. The average duration of the plasticity also varied across studies from less than 10 min to more than 1 hour.
27. Platinum bipolar stimulating electrodes were lowered 7 mm below the cortical surface 3.3 mm lateral and 2.3 mm posterior to the bregma in barbiturate-anesthetized rats weighing ∼300 g and were cemented into place with the use of sterile techniques approved under animal care protocol of the University of California, San Francisco. After 2 weeks of recovery, 250-ms (or a 15-Hz train of six 25-ms) 50-dB sound pressure level tones were paired with 200 ms of NB electrical stimulation in a sound-shielded, calibrated test chamber (5 days per week). Electrical stimulation began either 50 ms after tone onset (n = 15) or 200 ms before (n = 6). The two timings did not appear to affect plasticity, and data from both groups were pooled. The current level (70 to 150 μA) was chosen to be the minimum necessary to desynchronize the EEG during slow-wave sleep for 1 to 2 s. Stimulation consisted of 100-Hz capacitatively coupled biphasic pulses of 0.1 ms duration. Tonal and electrical stimuli did not evoke any observable behavioral responses (that is, did not cause rats to stop grooming or if sleeping, awaken).
28. Twenty-four hours after the last pairing, animals were anesthetized with pentobarbital and the right auditory cortex was surgically exposed. Parylene-coated tungsten microelectrodes (2 megohms) were lowered 550 μm below the pial surface (layer 4/5), and complete tuning curves were generated with 50-ms pure tones (with 3-ms ramps) presented at 2 Hz to the contralateral ear. The evoked spikes of a small cluster of neurons were collected at each site. To determine the effects of conditioning on the bandwidth of individual neurons, spike waveforms were collected during eight experiments and were sorted offline with software from Brainwave Technologies. Penetration locations were referenced using the cortical vasculature as landmarks. The primary auditory cortex was defined on the basis of its short latency (8-to 20-ms) responses and continuous tonotopy (BF increases from posterior to anterior). Responsive sites that exhibited clearly discontinuous BFs and either long latency responses, an unusually high threshold, or very broad tuning were considered to be non-A1 sites. Penetration sites were chosen to avoid blood vessels while generating a detailed and evenly spaced map. The edges of the map were estimated with the use of a line connecting the nonresponsive and non-A1 sites. Map reorganizations resulted in significant effects on the outline of A1, although no particular pattern was observed. The effect of conditioning on mean bandwidths across all conditions was determined with analysis of variance; pairwise comparisons were analyzed by Bonferroni post-hoc tests.
29. The set of tone frequencies presented at each site was approximately centered on the BF of each site. Thus, during analysis each tuning curve was approximately centered in the stimulus space, and simply blanking the axes and analyzing the sites in random order allowed for tuning curve characterization to be completely blind. With the use of custom analysis software, the tuning curve edges for each site were defined by hand and recorded without the possibility of experimenter bias.
30. S. L. Sally and J. B. Kelly, J. Neurophysiol. 59, 1627 (1988).
31. G. H. Recanzone, C. E. Schreiner, M. M. Merzenich, J. Neurosci. 13, 87 (1993).
32. W. M. Jenkins, M. M. Merzenich, M. T. Ochs, T. Allard, E. Guic-Robles, J. Neurophysiol. 63, 82 (1990).
33. G. H. Recanzone, M. M. Merzenich, W. M. Jenkins, K. A. Grajski, H. R. Dinse, ibid. 67, 1031 (1992).
34. M. P. Kilgard and M. M. Merzenich, unpublished observation.
35. In contrast to the large changes induced by pairing tones with NB stimulation, no significant cortical map reorganizations were observed in previous experiments after tens of thousands of behaviorally irrelevant stimuli were presented over 3 to 5 months (14, 16). Additionally, short-term repetition of one frequency without behavioral relevance (habituation) results in a dramatic decrease in A1 responses to that frequency [C. D. Condon and N. M. Weinberger, Behav. Neurosci. 105, 416 (1991)]. These studies suggest that stimulus presentation without behavioral importance does not result in significant map changes. Although it is unlikely to be a contributing factor, we acknowledge that we did not record from animals that experienced extensive stimulus presentation without any NB stimulation.
36. F. Casamenti, G. Deffenu, A. L. Abbamondi, G. Pepeu, Brain Res. Bull. 16, 689 (1986); D. D. Rasmusson, K. Clow, J. C. Szerb, Brain Res. 594, 150 (1992); M. E. Jimenez-Capdeville, R. W. Dykes, A. A. Myasnikov, J. Comp. Neurol. 381, 53 (1997).
37. F. Casamenti, G. Deffenu, A. L. Abbamondi, G. Pepeu, Brain Res. Bull. 16, 689 (1986); D. D. Rasmusson, K. Clow, J. C. Szerb, Brain Res. 594, 150 (1992); M. E. Jimenez-Capdeville, R. W. Dykes, A. A. Myasnikov, J. Comp. Neurol. 381, 53 (1997).
38. F. Casamenti, G. Deffenu, A. L. Abbamondi, G. Pepeu, Brain Res. Bull. 16, 689 (1986); D. D. Rasmusson, K. Clow, J. C. Szerb, Brain Res. 594, 150 (1992); M. E. Jimenez-Capdeville, R. W. Dykes, A. A. Myasnikov, J. Comp. Neurol. 381, 53 (1997).
39. B. Hars, C. Maho, J. M. Edeline, E. Hennevin, Neuroscience 56, 61 (1993); J. S. Bakin and N. M. Weinberger, Proc. Natl. Acad. Sci. U.S.A. 93, 11219 (1996).
40. B. Hars, C. Maho, J. M. Edeline, E. Hennevin, Neuroscience 56, 61 (1993); J. S. Bakin and N. M. Weinberger, Proc. Natl. Acad. Sci. U.S.A. 93, 11219 (1996).
41. The cholinergic neurons of the NB were selectively destroyed by infusion of 2.5 μg of 192 immunoglobulin G-saporin immunotoxin into the right lateral ventricle before the surgery to implant the stimulating electrode. The toxin, an antibody to the low-affinity nerve growth factor receptor linked to a ribosome-inactivating toxin, has been shown to specifically destroy most of the cholinergic neurons of the basal forebrain projecting to the cortex, while sparing the parvalbumin-containing neurons as well as cholinergic neurons that project from the NB to the amygdala [S. Heckers et al., J. Neurosci. 14, 1271 (1994)]. Electrical stimulation of the NB and tone presentation were identical for lesioned and nonlesioned animals. The percent of the cortex responding to a 19-kHz tone after pairing in lesioned animals was not significantly different from that in naïve controls (two-tailed t test, n = 2).
42. I. Gritti, L. Mainville, M. Mancia, B. E. Jones, J. Comp. Neurol. 383, 163 (1997).
43. Complex considerations of the network, cellular, and molecular mechanisms responsible for the plasticity observed in our studies are beyond the scope of this report. See M. E. Hasselmo and J. M. Bower, Trends Neurosci. 16, 218 (1993); M. Sarter and J. P. Bruno, Brain Res. Rev. 23, 28 (1997); R. W. Dykes, Can. J. Physiol. Pharmacol. 75, 535 (1997).
44. Complex considerations of the network, cellular, and molecular mechanisms responsible for the plasticity observed in our studies are beyond the scope of this report. See M. E. Hasselmo and J. M. Bower, Trends Neurosci. 16, 218 (1993); M. Sarter and J. P. Bruno, Brain Res. Rev. 23, 28 (1997); R. W. Dykes, Can. J. Physiol. Pharmacol. 75, 535 (1997).
45. Complex considerations of the network, cellular, and molecular mechanisms responsible for the plasticity observed in our studies are beyond the scope of this report. See M. E. Hasselmo and J. M. Bower, Trends Neurosci. 16, 218 (1993); M. Sarter and J. P. Bruno, Brain Res. Rev. 23, 28 (1997); R. W. Dykes, Can. J. Physiol. Pharmacol. 75, 535 (1997).
46. Supported by NIH grant NS-10414, Hearing Research Inc., and an NSF predoctoral fellowship. We thank C. Schreiner for technical advice and D. Buonomano, H. Mahncke, D. Blake, C. deCharms, C. Schreiner, and K. Miller for helpful comments on the manuscript.