Short-term plasticity of a thalamocortical pathway dynamically modulated by behavioral state

Science

Volumn 272, Issue 5259, 1996, Pages 274-277

  Castro Alamancos, Manuel A ^a   Connors, Barry W ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; THALAMOCORTICAL TRACT; THALAMUS;

EID: 0029670288     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5259.274     Document Type: Article

References (33)

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3. E. W Dempsey and R. S. Morison, Am. J. Physiol. 138, 283 (1943); R. S Monson and E W. Dempsey, ibid., p. 297. Augmenting responses are neocortical field potentials, characteristically surface positive and middle-layer negative, that increase in size during paired or multiple stimuli applied at 8 to 15 Hz; steady state is reached by the third response. Augmenting responses should not be confused with recruiting responses, which are surface negative and middle-layer positive and are induced by stimulating thalamic nuclei that project to neocortical layer I [L. L. Glenn, J Hada, J P. Roy, M. Deschenes, M. Steriade, Neuroscience 7, 1861 (1982); M Herkenham, in (1), pp. 403-446], nor with a different form of short-term synaptic plasticity commonly known as augmentation [ R. S. Zucker, Annu. Rev. Neurosci. 12, 13 (1989)].
4. E. W Dempsey and R. S. Morison, Am. J. Physiol. 138, 283 (1943); R. S Monson and E W. Dempsey, ibid., p. 297. Augmenting responses are neocortical field potentials, characteristically surface positive and middle-layer negative, that increase in size during paired or multiple stimuli applied at 8 to 15 Hz; steady state is reached by the third response. Augmenting responses should not be confused with recruiting responses, which are surface negative and middle-layer positive and are induced by stimulating thalamic nuclei that project to neocortical layer I [L. L. Glenn, J Hada, J P. Roy, M. Deschenes, M. Steriade, Neuroscience 7, 1861 (1982); M Herkenham, in (1), pp. 403-446], nor with a different form of short-term synaptic plasticity commonly known as augmentation [ R. S. Zucker, Annu. Rev. Neurosci. 12, 13 (1989)].
5. E. W Dempsey and R. S. Morison, Am. J. Physiol. 138, 283 (1943); R. S Monson and E W. Dempsey, ibid., p. 297. Augmenting responses are neocortical field potentials, characteristically surface positive and middle-layer negative, that increase in size during paired or multiple stimuli applied at 8 to 15 Hz; steady state is reached by the third response. Augmenting responses should not be confused with recruiting responses, which are surface negative and middle-layer positive and are induced by stimulating thalamic nuclei that project to neocortical layer I [L. L. Glenn, J Hada, J P. Roy, M. Deschenes, M. Steriade, Neuroscience 7, 1861 (1982); M Herkenham, in (1), pp. 403-446], nor with a different form of short-term synaptic plasticity commonly known as augmentation [ R. S. Zucker, Annu. Rev. Neurosci. 12, 13 (1989)].
6. E. W Dempsey and R. S. Morison, Am. J. Physiol. 138, 283 (1943); R. S Monson and E W. Dempsey, ibid., p. 297. Augmenting responses are neocortical field potentials, characteristically surface positive and middle-layer negative, that increase in size during paired or multiple stimuli applied at 8 to 15 Hz; steady state is reached by the third response. Augmenting responses should not be confused with recruiting responses, which are surface negative and middle-layer positive and are induced by stimulating thalamic nuclei that project to neocortical layer I [L. L. Glenn, J Hada, J P. Roy, M. Deschenes, M. Steriade, Neuroscience 7, 1861 (1982); M Herkenham, in (1), pp. 403-446], nor with a different form of short-term synaptic plasticity commonly known as augmentation [ R. S. Zucker, Annu. Rev. Neurosci. 12, 13 (1989)].
7. W. A. Spencer and J. M. Brookhart, J. Neurophysiol. 24, 26 (1961), D. P Purpura and R. J. Shofer, ibid. 27, 117 (1964); K. Sasaki, H. P. Staunton, G. Dieckmann, Exp Neurol 26, 369 (1970).
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12. Explanations have included origins in the thalamus (3) and the cortex (5)
13. Sprague-Dawley rats (250 to 350 g) were anesthetized with ketamine HCl (100 mg per kilogram of body weight, intraperitoneally) and regularly supplemented (50 mg/kg, intramuscularly). After induction of surgical anesthesia, the animal was placed in a stereotaxic frame. All skin incisions and frame contacts with the skin were injected with lidocaine (2%). A unilateral craniotomy extended over a large area of the parietofrontal cortex Small incisions were made in the dura as necessary, and the cortical surface was covered with saline. Body temperature was monitored and maintained constant with a heating pad. Thalamus-stimulating electrodes were inserted with stereotaxic procedures {all coordinates are given in millimeters, in reference to the bregma and the dura [G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates (Academic Press, New York, 1982)]}. Coordinates for the VL were approximately (in millimeters) anterior-postenor = -2 0, lateral = 2.0; and depth = 5.5. Stimulus current intensity was selected to induce a stable response (<200 μA), and pulses were monophasic and of 200-μs duration Twisted, insulated bipolar stainless steel electrodes were used for stimulating the thalamus. Recording electrodes were placed within the following region: anterior-posterior = 0 to 1 mm, and lateral = 3 to 4 mm. Extracellular recording electrodes were Teflon-insulated platinum-iridium wires (0.007-inch diameter, 0 005-inch tip size). For GSD analysis, 20 responses were averaged from each depth, with averages taken at 100-μm intervals from the pial surface to a depth of 2000 CSDs were calculated by approximating the second spatial derivative of voltage with methods previously described [ U. Mitzdorf, Physiol. Rev. 65, 37 (1985)] To ensure stability of the preparation during long recording sessions, we did the following: (i) the moving electrode was always returned to the initial recording depths, (ii) measurements from that site were repeated to check that no significant change had occurred, and (iii) the electrocorticogram was continuously monitored for stability. Electrophysiological responses were sampled at 10 kHz and stored on a computer with Experimenter's Workbench (Data Wave Technologies). Analysis was performed with Experimenter's Workbench and Origin (Microcal Software) At the end of each experiment, marking lesions were placed at the thalamic locations that had served as stimulating sites. The animals were given an overdose of sodium pentobarbital, and the brain was extracted and placed in a fixative solution (5% paraformaldehyde in saline). Subsequently, slices of the frontoparietal cortex and thalamus were cut with a vibratome and stained for Nissl. Protocols for all experiments were approved by the Brown University Institutional Animal Care and Use Committee.
14. Sprague-Dawley rats (250 to 350 g) were anesthetized with ketamine HCl (100 mg per kilogram of body weight, intraperitoneally) and regularly supplemented (50 mg/kg, intramuscularly). After induction of surgical anesthesia, the animal was placed in a stereotaxic frame. All skin incisions and frame contacts with the skin were injected with lidocaine (2%). A unilateral craniotomy extended over a large area of the parietofrontal cortex Small incisions were made in the dura as necessary, and the cortical surface was covered with saline. Body temperature was monitored and maintained constant with a heating pad. Thalamus-stimulating electrodes were inserted with stereotaxic procedures {all coordinates are given in millimeters, in reference to the bregma and the dura [G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates (Academic Press, New York, 1982)]}. Coordinates for the VL were approximately (in millimeters) anterior-postenor = -2 0, lateral = 2.0; and depth = 5.5. Stimulus current intensity was selected to induce a stable response (<200 μA), and pulses were monophasic and of 200-μs duration Twisted, insulated bipolar stainless steel electrodes were used for stimulating the thalamus. Recording electrodes were placed within the following region: anterior-posterior = 0 to 1 mm, and lateral = 3 to 4 mm. Extracellular recording electrodes were Teflon-insulated platinum-iridium wires (0.007-inch diameter, 0 005-inch tip size). For GSD analysis, 20 responses were averaged from each depth, with averages taken at 100-μm intervals from the pial surface to a depth of 2000 CSDs were calculated by approximating the second spatial derivative of voltage with methods previously described [ U. Mitzdorf, Physiol. Rev. 65, 37 (1985)] To ensure stability of the preparation during long recording sessions, we did the following: (i) the moving electrode was always returned to the initial recording depths, (ii) measurements from that site were repeated to check that no significant change had occurred, and (iii) the electrocorticogram was continuously monitored for stability. Electrophysiological responses were sampled at 10 kHz and stored on a computer with Experimenter's Workbench (Data Wave Technologies). Analysis was performed with Experimenter's Workbench and Origin (Microcal Software) At the end of each experiment, marking lesions were placed at the thalamic locations that had served as stimulating sites. The animals were given an overdose of sodium pentobarbital, and the brain was extracted and placed in a fixative solution (5% paraformaldehyde in saline). Subsequently, slices of the frontoparietal cortex and thalamus were cut with a vibratome and stained for Nissl. Protocols for all experiments were approved by the Brown University Institutional Animal Care and Use Committee.
15. Recordings were made from a grid of 24 equally spaced (1 mm apart) penetrations across the frontoparietal neocortex of the rat Figure 1E shows the amplitude of the negative field potential recorded in the depth (1500 μm) of the cortex in response to the first and second pulse delivered to the VL with an interstimulus interval of 100 ms.
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17. Procedures for implanting electrodes in freely moving animals have been described [M. A. Castro-Alamancos and J. Borrell, Neuroscience 68, 793 (1995)]. Electrophysiological recordings were performed as in anesthetized animals, but with field effect transistors (NBLABS, Dennison, TX) attached to the recording electrodes within the animal's head connector. During recording sessions an animal was placed in an open field (43 2 cm by 43.2 cm) containing two arrays of 16 photobeams (Med Associates, Georgia, VT) that detected any movements performed by the animal in the open field. Electrophysiological recordings, motor activity consisting of 10-ms pulses signaling the interruption of a photobeam, and the experimenter's observations were fed into a video tape recording system (Neurodata Instruments, New York, NY) and to Experimenter's Workbench. Three awake behavioral states were easily distinguished. During the immobility state the animal was standing still with eyes open and fixed (photobeams were not interrupted). Immobility preceded the onset of the exploration state, during which the animal moved around and explored the environment (large numbers of photobeam interruptions are recorded). Finally, during the resting state the animal was lying down in the cage, typically in one corner, with eyes open (no photobeam counts were detected) The resting state was easily distinguished from immobility by visual observation and by the long period of associated photobeam silence, whereas during immobility, phasic periods of photobeam silence were interrupted by periods of exploration.
18. Animals had been trained in a motor skill grasping task [M A Castro-Alamancos and J. Borrell, Neuroscience 52, 637 (1993)] for several days before being implanted with stimulating and recording electrodes. During the recording sessions the animals were allowed to grasp food pellets for a continuous session of 10 to 15 min. While food was accessible, the animals were very actively engaged in reaching into the tube, grasping and retrieving food pellets, and placing the pellets into their mouths, and immobility did not occur.
19. M. A. Castro-Alamancos and B W. Connors, J. Neurosci. 16, 2767 (1996)
20. Intracellular (conventional sharp-type) recording electrodes were filled with 3 M potassium acetate (80 to 120 megaohms), recordings were made from cells of different cortical layers (n = 41), and procedures were similar to those used for slices [M. A Castro-Alamancos, J P Donoghue, B. W. Connors, J. Neurosci. 15, 5324 (1995)].
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33. Supported by fellowships to M.A.C. from the Ministry of Science and Education of Spain and the National Institute of Mental Health (MH19118), and grants to B.W.C. from the NIH (NS25983) and the Office of Naval Research (N00014-90-J-1701).