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Effects of a dorsal column lesion on temporal processing within the somatosensory system of primates

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Abstract

A dorsal column (DC) lesion has lasting effects on behavioral tasks that require temporal processing of tactile information (e.g., frequency and duration discrimination). The present experiments describe physiological correlates of these deficits in temporal discrimination. Compound action potentials evoked by electrocutaneous stimulation were recorded from the major white matter subdivisions of the spinal cord in anesthetized monkeys, and relationships between stimulation frequency and evoked potential (EP) amplitude were determined for the ascending pathways. At 10 pulses per second (Hz) EPs recorded in the lateral spinal columns were attenuated slightly (by 15% or less, relative to 1.5 Hz), whereas potentials recorded from the DCs were not attenuated. The attenuation increased with stimulation frequencies up to 50 Hz, reaching 80% for the anterolateral column and 38% for the dorsolateral column, but only 15% for the DC. Epidural EPs were recorded, before and after interruption of the contralateral DC, from awake animals with electrodes chronically implanted over primary somatosensory cortex (SI). Following the lesion, EP responses to 1.5-Hz stimulation were 46% of preoperative responses to the same stimulus. At 10 Hz, EP amplitudes were attenuated even more, to 27% of the preoperative amplitude at 1.5 Hz. Principal components analysis was employed to quantify alterations in EP conformation and stimulus frequency was varied from 1.5 to 10 Hz, before and after a DC lesion. Interruption of the DC resulted in a significant decrease in the information provided by the EP about changes in stimulus frequency. EPs were also recorded from different locations along the anterior-posterior dimension of the hindlimb region of SI in lightly anesthetized animals. Principal components analysis revealed that there was less information present in the EP about changes in stimulus frequency (1.5–10 Hz) at all recording locations in animals with a DC lesion, compared with the cortex of normal animals. The DC lesion significantly decreased the amplitude of cortical EPs evoked by repetitive stimulation. At 10 Hz the EP was nearly buried in noise, consistent with behavioral deficits in discrimination of the duration of 10 Hz stimulation following interruption of the DC. Also, significantly less information was present in the cortical EPs about changes in stimulus frequency in the absence of intact DCs, which is consistent with deficits in frequency discrimination. This reduction could be explained in part by a lesser capacity of spinal pathways in the lateral column to follow repetitive stimulation above 10 Hz. However, more rostral manifestations of a DC lesion, at either the thalamus or the cortex, are likely to contribute to the reduced capacity of animals with DC lesions to make temporal discriminations.

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Authors and Affiliations

  1. Department of Neuroscience, University of Florida, P.O. Box 100244, 32610, Gainesville, FL, USA

    James C. Makous, Robert M. Friedman & Charles J. Vierck Jr.

  2. Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8108, 63110-1093, St. Louis, MO, USA

    James C. Makous

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  3. Charles J. Vierck Jr.
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Makous, J.C., Friedman, R.M. & Vierck, C.J. Effects of a dorsal column lesion on temporal processing within the somatosensory system of primates. Exp Brain Res 112, 253–267 (1996). https://doi.org/10.1007/BF00227644

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  • DOI: https://doi.org/10.1007/BF00227644

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