SI neuron response variability is stimulus tuned and NMDA receptor dependent

B. L. Whitsel, O. Favorov, K. A. Delemos, Changjoon Lee, M. Tommerdahl, G. K. Essick, B. Nakhle

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Skin brushing stimuli were used to evoke spike discharge activity in single skin mechanoreceptive afferents (sMRAs) and anterior parietal cortical (SI) neurons of anesthetized monkeys (Macaca fascicularis). In the initial experiments 10-50 presentations of each of 8 different stimulus velocities were delivered to the linear skin path from which maximal spike discharge activity could be evoked. Mean rate of spike firing evoked by each velocity (MFR) was computed for the time period during which spike discharge activity exceeded background, and an across-presentations estimate of mean firing rate (M̄F̄R̄) was generated for each velocity. The magnitude of the trial-by- trial variation in the response (estimated as CV; where CV = standard deviation in MFR/M̄F̄R̄) was determined for each unit at each velocity. M̄F̄R̄ for both sMRAs and SI neurons (M̄F̄R̄(sMRA) and M̄F̄R̄(SI), respectively) increased monotonically with velocity over the range 1-100 cm/s. At all velocities the average estimate of intertrial response variation for SI neurons (C̄V̄(SI)) was substantially larger than the corresponding average for sMRAs (C̄V̄(sMRA)). Whereas C̄V̄(sMRA) increased monotonically over the range 1-100 cm/s, C̄V̄(SI) decreased progressively with velocity over the range 1-10 cm/s, and then increased with velocity over the range 10-100 cm/s. The position of the skin brushing stimulus in the receptive field (RF) was varied in the second series of experiments. It was found that the magnitude of CV(SI) varied systematically with stimulus position in the RF: that is, CV(SI) was lowest for a particular velocity and direction of stimulus motion when the skin brushing stimulus traversed the RF center, and CV(SI) increased progressively as the distance between the stimulus path and the RF center increased. In the third series of experiments, either phencylidine (PCP; 100-500 μg/kg) or ketamine (KET; 0.57.5 mg/kg) was administered intravenously (iv) to assess the effect of block of N-methyl-D-aspartate (NMDA) receptors on SI neuron intertrial response variation. The effects of PCP on both CV(SI) and M̄F̄R̄(SI) were transient, typically with full recovery occurring in 1-2 h after drug injection. The effects of KET on CV(SI) and M̄F̄R̄(SI) were similar to those of PCP, but were shorter in duration (15-30 min). PCP and KET administration consistently was accompanied by a reduction of CV(SI). The magnitude of the reduction of CV(SI) by PCP or KET was associated with the magnitude of CV(SI) before drug administration: that is, the larger the predrug CV(SI), the larger the reduction in CV(SI) caused by PCP or KET. PCP and KET exerted variable effects on SI neuron mean firing rate that could differ greatly from one neuron to the next. The results are interpreted to indicate that SI neuron intertrial response variation is 1) stimulus tuned (intertrial response variation is lowest when the skin stimulus moves at 10 cm/s and traverses the neuron's RF center) and 2) NMDA receptor dependent (intertrial response variation is least when NMDA receptor activity contributes minimally to the response, and increases as the contribution of NMDA receptors to the response increases).

Original languageEnglish
Pages (from-to)2988-3006
Number of pages19
JournalJournal of Neurophysiology
Volume81
Issue number6
Publication statusPublished - 1999
Externally publishedYes

Fingerprint

N-Methyl-D-Aspartate Receptors
Neurons
Skin
Afferent Neurons
Macaca fascicularis
Ketamine
Pharmaceutical Preparations
Haplorhini
Injections

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Whitsel, B. L., Favorov, O., Delemos, K. A., Lee, C., Tommerdahl, M., Essick, G. K., & Nakhle, B. (1999). SI neuron response variability is stimulus tuned and NMDA receptor dependent. Journal of Neurophysiology, 81(6), 2988-3006.

SI neuron response variability is stimulus tuned and NMDA receptor dependent. / Whitsel, B. L.; Favorov, O.; Delemos, K. A.; Lee, Changjoon; Tommerdahl, M.; Essick, G. K.; Nakhle, B.

In: Journal of Neurophysiology, Vol. 81, No. 6, 1999, p. 2988-3006.

Research output: Contribution to journalArticle

Whitsel, BL, Favorov, O, Delemos, KA, Lee, C, Tommerdahl, M, Essick, GK & Nakhle, B 1999, 'SI neuron response variability is stimulus tuned and NMDA receptor dependent', Journal of Neurophysiology, vol. 81, no. 6, pp. 2988-3006.
Whitsel BL, Favorov O, Delemos KA, Lee C, Tommerdahl M, Essick GK et al. SI neuron response variability is stimulus tuned and NMDA receptor dependent. Journal of Neurophysiology. 1999;81(6):2988-3006.
Whitsel, B. L. ; Favorov, O. ; Delemos, K. A. ; Lee, Changjoon ; Tommerdahl, M. ; Essick, G. K. ; Nakhle, B. / SI neuron response variability is stimulus tuned and NMDA receptor dependent. In: Journal of Neurophysiology. 1999 ; Vol. 81, No. 6. pp. 2988-3006.
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abstract = "Skin brushing stimuli were used to evoke spike discharge activity in single skin mechanoreceptive afferents (sMRAs) and anterior parietal cortical (SI) neurons of anesthetized monkeys (Macaca fascicularis). In the initial experiments 10-50 presentations of each of 8 different stimulus velocities were delivered to the linear skin path from which maximal spike discharge activity could be evoked. Mean rate of spike firing evoked by each velocity (MFR) was computed for the time period during which spike discharge activity exceeded background, and an across-presentations estimate of mean firing rate (M̄F̄R̄) was generated for each velocity. The magnitude of the trial-by- trial variation in the response (estimated as CV; where CV = standard deviation in MFR/M̄F̄R̄) was determined for each unit at each velocity. M̄F̄R̄ for both sMRAs and SI neurons (M̄F̄R̄(sMRA) and M̄F̄R̄(SI), respectively) increased monotonically with velocity over the range 1-100 cm/s. At all velocities the average estimate of intertrial response variation for SI neurons (C̄V̄(SI)) was substantially larger than the corresponding average for sMRAs (C̄V̄(sMRA)). Whereas C̄V̄(sMRA) increased monotonically over the range 1-100 cm/s, C̄V̄(SI) decreased progressively with velocity over the range 1-10 cm/s, and then increased with velocity over the range 10-100 cm/s. The position of the skin brushing stimulus in the receptive field (RF) was varied in the second series of experiments. It was found that the magnitude of CV(SI) varied systematically with stimulus position in the RF: that is, CV(SI) was lowest for a particular velocity and direction of stimulus motion when the skin brushing stimulus traversed the RF center, and CV(SI) increased progressively as the distance between the stimulus path and the RF center increased. In the third series of experiments, either phencylidine (PCP; 100-500 μg/kg) or ketamine (KET; 0.57.5 mg/kg) was administered intravenously (iv) to assess the effect of block of N-methyl-D-aspartate (NMDA) receptors on SI neuron intertrial response variation. The effects of PCP on both CV(SI) and M̄F̄R̄(SI) were transient, typically with full recovery occurring in 1-2 h after drug injection. The effects of KET on CV(SI) and M̄F̄R̄(SI) were similar to those of PCP, but were shorter in duration (15-30 min). PCP and KET administration consistently was accompanied by a reduction of CV(SI). The magnitude of the reduction of CV(SI) by PCP or KET was associated with the magnitude of CV(SI) before drug administration: that is, the larger the predrug CV(SI), the larger the reduction in CV(SI) caused by PCP or KET. PCP and KET exerted variable effects on SI neuron mean firing rate that could differ greatly from one neuron to the next. The results are interpreted to indicate that SI neuron intertrial response variation is 1) stimulus tuned (intertrial response variation is lowest when the skin stimulus moves at 10 cm/s and traverses the neuron's RF center) and 2) NMDA receptor dependent (intertrial response variation is least when NMDA receptor activity contributes minimally to the response, and increases as the contribution of NMDA receptors to the response increases).",
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T1 - SI neuron response variability is stimulus tuned and NMDA receptor dependent

AU - Whitsel, B. L.

AU - Favorov, O.

AU - Delemos, K. A.

AU - Lee, Changjoon

AU - Tommerdahl, M.

AU - Essick, G. K.

AU - Nakhle, B.

PY - 1999

Y1 - 1999

N2 - Skin brushing stimuli were used to evoke spike discharge activity in single skin mechanoreceptive afferents (sMRAs) and anterior parietal cortical (SI) neurons of anesthetized monkeys (Macaca fascicularis). In the initial experiments 10-50 presentations of each of 8 different stimulus velocities were delivered to the linear skin path from which maximal spike discharge activity could be evoked. Mean rate of spike firing evoked by each velocity (MFR) was computed for the time period during which spike discharge activity exceeded background, and an across-presentations estimate of mean firing rate (M̄F̄R̄) was generated for each velocity. The magnitude of the trial-by- trial variation in the response (estimated as CV; where CV = standard deviation in MFR/M̄F̄R̄) was determined for each unit at each velocity. M̄F̄R̄ for both sMRAs and SI neurons (M̄F̄R̄(sMRA) and M̄F̄R̄(SI), respectively) increased monotonically with velocity over the range 1-100 cm/s. At all velocities the average estimate of intertrial response variation for SI neurons (C̄V̄(SI)) was substantially larger than the corresponding average for sMRAs (C̄V̄(sMRA)). Whereas C̄V̄(sMRA) increased monotonically over the range 1-100 cm/s, C̄V̄(SI) decreased progressively with velocity over the range 1-10 cm/s, and then increased with velocity over the range 10-100 cm/s. The position of the skin brushing stimulus in the receptive field (RF) was varied in the second series of experiments. It was found that the magnitude of CV(SI) varied systematically with stimulus position in the RF: that is, CV(SI) was lowest for a particular velocity and direction of stimulus motion when the skin brushing stimulus traversed the RF center, and CV(SI) increased progressively as the distance between the stimulus path and the RF center increased. In the third series of experiments, either phencylidine (PCP; 100-500 μg/kg) or ketamine (KET; 0.57.5 mg/kg) was administered intravenously (iv) to assess the effect of block of N-methyl-D-aspartate (NMDA) receptors on SI neuron intertrial response variation. The effects of PCP on both CV(SI) and M̄F̄R̄(SI) were transient, typically with full recovery occurring in 1-2 h after drug injection. The effects of KET on CV(SI) and M̄F̄R̄(SI) were similar to those of PCP, but were shorter in duration (15-30 min). PCP and KET administration consistently was accompanied by a reduction of CV(SI). The magnitude of the reduction of CV(SI) by PCP or KET was associated with the magnitude of CV(SI) before drug administration: that is, the larger the predrug CV(SI), the larger the reduction in CV(SI) caused by PCP or KET. PCP and KET exerted variable effects on SI neuron mean firing rate that could differ greatly from one neuron to the next. The results are interpreted to indicate that SI neuron intertrial response variation is 1) stimulus tuned (intertrial response variation is lowest when the skin stimulus moves at 10 cm/s and traverses the neuron's RF center) and 2) NMDA receptor dependent (intertrial response variation is least when NMDA receptor activity contributes minimally to the response, and increases as the contribution of NMDA receptors to the response increases).

AB - Skin brushing stimuli were used to evoke spike discharge activity in single skin mechanoreceptive afferents (sMRAs) and anterior parietal cortical (SI) neurons of anesthetized monkeys (Macaca fascicularis). In the initial experiments 10-50 presentations of each of 8 different stimulus velocities were delivered to the linear skin path from which maximal spike discharge activity could be evoked. Mean rate of spike firing evoked by each velocity (MFR) was computed for the time period during which spike discharge activity exceeded background, and an across-presentations estimate of mean firing rate (M̄F̄R̄) was generated for each velocity. The magnitude of the trial-by- trial variation in the response (estimated as CV; where CV = standard deviation in MFR/M̄F̄R̄) was determined for each unit at each velocity. M̄F̄R̄ for both sMRAs and SI neurons (M̄F̄R̄(sMRA) and M̄F̄R̄(SI), respectively) increased monotonically with velocity over the range 1-100 cm/s. At all velocities the average estimate of intertrial response variation for SI neurons (C̄V̄(SI)) was substantially larger than the corresponding average for sMRAs (C̄V̄(sMRA)). Whereas C̄V̄(sMRA) increased monotonically over the range 1-100 cm/s, C̄V̄(SI) decreased progressively with velocity over the range 1-10 cm/s, and then increased with velocity over the range 10-100 cm/s. The position of the skin brushing stimulus in the receptive field (RF) was varied in the second series of experiments. It was found that the magnitude of CV(SI) varied systematically with stimulus position in the RF: that is, CV(SI) was lowest for a particular velocity and direction of stimulus motion when the skin brushing stimulus traversed the RF center, and CV(SI) increased progressively as the distance between the stimulus path and the RF center increased. In the third series of experiments, either phencylidine (PCP; 100-500 μg/kg) or ketamine (KET; 0.57.5 mg/kg) was administered intravenously (iv) to assess the effect of block of N-methyl-D-aspartate (NMDA) receptors on SI neuron intertrial response variation. The effects of PCP on both CV(SI) and M̄F̄R̄(SI) were transient, typically with full recovery occurring in 1-2 h after drug injection. The effects of KET on CV(SI) and M̄F̄R̄(SI) were similar to those of PCP, but were shorter in duration (15-30 min). PCP and KET administration consistently was accompanied by a reduction of CV(SI). The magnitude of the reduction of CV(SI) by PCP or KET was associated with the magnitude of CV(SI) before drug administration: that is, the larger the predrug CV(SI), the larger the reduction in CV(SI) caused by PCP or KET. PCP and KET exerted variable effects on SI neuron mean firing rate that could differ greatly from one neuron to the next. The results are interpreted to indicate that SI neuron intertrial response variation is 1) stimulus tuned (intertrial response variation is lowest when the skin stimulus moves at 10 cm/s and traverses the neuron's RF center) and 2) NMDA receptor dependent (intertrial response variation is least when NMDA receptor activity contributes minimally to the response, and increases as the contribution of NMDA receptors to the response increases).

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