SI neuron response variability is stimulus tuned and NMDA receptor dependent

Department of Cell and Molecular Physiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 07/1999; 81(6):2988-3006.
Source: PubMed


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 (MFR) 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/MFR) was determined for each unit at each velocity. MFR for both sMRAs and SI neurons (MFRsMRA and MFRSI, 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 (CVSI) was substantially larger than the corresponding average for sMRAs (CVsMRA). Whereas CVsMRA increased monotonically over the range 1-100 cm/s, CVSI 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 CVSI varied systematically with stimulus position in the RF: that is, CVSI was lowest for a particular velocity and direction of stimulus motion when the skin brushing stimulus traversed the RF center, and CVSI 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 microg/kg) or ketamine (KET; 0.5-7.5 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 CVSI and MFRSI were transient, typically with full recovery occurring in 1-2 h after drug injection. The effects of KET on CVSI and MFRSI 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 CVSI. The magnitude of the reduction of CVSI by PCP or KET was associated with the magnitude of CVSI before drug administration: that is, the larger the predrug CVSI, the larger the reduction in CVSI 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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    • "high-frequency vibrotactile stimulation. Specifically, although SI remains activated (and presumably, therefore, fully responsive) for the full duration of 25 Hz stimulation, it undergoes a profound suppression/inhibition within 1–2 s of the onset of 200 Hz stimulation (Tommerdahl et al., 1999a,b; Whitsel et al., 1999, 2000, 2001). The adaptation-induced impairment of human vibrotactile frequency discrimination reported by Tommerdahl et al. (2005c) is regarded as fully consistent with the idea that antagonistic interactions (''cross-channel interactions'') can and frequently do occur between the CNS processes triggered by activity in the ascending projections of both the RA-1 (also referred to as FAI) and PC (FAII) mechanoreceptive afferents. "
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    ABSTRACT: Neural representation of somatosensory events undergoes major transformation in the primary somatosensory cortex (SI) from its original, more or less isomorphic, form found at the level of peripheral receptors. A large body of SI optical imaging, neural recording and psychophysical studies suggests that SI representation of stimuli encountered in everyday life is a product of dynamic processes that involve competitive interactions at multiple levels of cortical organization. Such interactions take place among neighboring neurons, among local groups of minicolumns, among neighboring macrocolumns, between SI and SII, between Pacinian and non-Pacinian channels, and bilaterally between homotopic somatosensory regions of the opposite hemispheres. Together these interactions sharpen SI response to suprathreshold and time-extended tactile stimuli by funneling the initially widespread stimulus-triggered activity in SI into the local group of macrocolumns most directly driven by the stimulus. Those macrocolumns in turn fractionate into stimulus-specific patterns of differentially active minicolumns. Thus SI dynamically shapes its representation of a tactile stimulus by selecting among all of its neurons initially activated by the stimulus a subset of neurons with receptive-field and feature-tuning properties closely matching those of the stimulus. Through this stimulus-directed dynamical selection process, which operates on a scale of hundreds of milliseconds, SI achieves a more faithful representation of stimulus properties, which is reflected in improved performance on tactile perceptual tasks.
    Full-text · Article · Oct 2009 · Neuroscience & Biobehavioral Reviews
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    • "For example, although N-methyl-D-aspartate receptor (NMDAR) block in the nonhuman primate results in decreased overall mean firing rate, a contraction of receptive fields, a reduction in the variability of the cortical response, and a decreased spatial extent in the cortical response evoked by tactile stimulation [3,4], little is known about the somatosensory perceptual correlates of NMDAR block. One finding of interest in the nonhuman primate studies is that NMDAR block results in a decrease in the change in responsiveness with repetitive stimulation [4]. In other words, whereas the majority of primary somatosensory cortical neurons show a significant decrease in overall mean firing rate evoked by repetitive vibrotactile stimulation, the application of NMDAR block results in the majority of these same neurons exhibiting an absence of this change in overall mean firing rate. "
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    ABSTRACT: Previous reports have demonstrated that short durations of vibrotactile stimuli (less than or equal to 2 sec) effectively and consistently modify both the perceptual response in humans as well as the neurophysiological response in somatosensory cortex. The change in cortical response with adaptation has been well established by a number of studies, and other reports have extended those findings in determining that both GABA- and NMDAR-mediated neurotransmission play a significant role in the dynamic response of somatosensory cortical neurons. In this study, we evaluated the impact that dextromethorphan (DXM), an NMDAR antagonist, had on two distinct vibrotactile adaptation tasks. All subjects, both those that ingested 60 mg DXM and those that ingested placebo, were evaluated for their amplitude discriminative capacity between two simultaneously delivered vibrotactile stimuli both with and without 3 conditions of pre-exposure to adapting stimulation. The results demonstrated that the perceptual metrics of subjects who ingested 60 mg DXM were significantly altered from that of controls when the amplitude discrimination task followed one of the conditions of adapting stimulation. Without the condition of pre-exposure to an adapting stimulus (or stimuli), there was little difference between the observations obtained from the subjects that ingested DXM and controls. Peak impact on subject response occurred at 60 min post-ingestion, whereas the scores of controls who ingested placebo were not impacted. The results - that DXM blocks vibrotactile adaptation - is consistent with the suggestion that NMDAR-mediated neurotransmission plays a significant role in the perceptual adaptive response. This finding is also consistent with neurophysiological findings that report observations of the effects of NMDAR block on the SI cortical response to repetitive vibrotactile stimulation.
    Full-text · Article · Oct 2008 · BMC Neuroscience
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