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Tactile Coactivation-Induced Changes in Spatial Discrimination Performance

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Tactile Coactivation-Induced Changes in Spatial Discrimination Performance The Journal of Neuroscience, February 15, 2000, 20(4):1597–1604 Tactile Coactivation-Induced Changes in Spatial Discrimination Performance Ben Godde,1 Beate Stauffenberg,2 Friederike Spengler,2 and Hubert R. Dinse2 1Institute of Medical Psychology, University of Tu¨ bingen, 72074 Tu¨ bingen, Germany, and 2Institute of Neuroinformatics, Theoretical Biology, Ruhr-University of Bochum, ND04, 44780 Bochum, Germany We studied coactivation-based cortical plasticity at a psycho- coactivation protocol revealed that 30 min was not sufficient to physical level in humans. For induction of plasticity, we used a drive plastic changes. Repeated application of coactivation protocol of simultaneous pairing of tactile stimulation to follow over 3 consecutive days resulted in a delayed recovery indicat- as closely as possible the idea of Hebbian learning. We re- ing stabilization of the improvement over time. Perceptual ported previously that a few hours of tactile coactivation re- changes were highly selective because no transfer of improved sulted in selective and reversible reorganization of receptive performance to fingers that were not stimulated was found. The fields and cortical maps of the hindpaw representation of the results demonstrate the potential role of sensory input statistics somatosensory cortex of adult rats (Godde et al., 1996). In the (i.e., their probability of occurrence and spatiotemporal relation- present study, simultaneous spatial two-point discrimination ships) in the induction of cortical plasticity without involving was tested on the tip of the right index finger in human subjects cognitive factors such as attention or reinforcement. as a marker of plastic changes. After 2 hr of coactivation we Key words: coactivation; associative pairing; somatosensory; found a significant improvement in discrimination performance tactile; perceptual learning; humans; cortical reorganization; that was reversible within 8 hr. Reduction of the duration of the plasticity; Hebbian learning; attention Training and learning induce powerful reorganizational changes, To study the effects of variation of input statistics, we intro- which are referred to as use- or experience-dependent plasticity. duced a paradigm of coactivation in which temporally coherent In owl monkeys, Recanzone et al. (1992b) demonstrated a direct inputs were generated by the simultaneous pairing of tactile relation between cortical plastic changes and improvement of stimuli (Godde et al., 1996). In this initial study we demonstrated psychophysically assessed performance. The recent development that the simultaneous coactivation protocol was able to induce of noninvasive-imaging techniques made it possible to study in within a few hours reversible reorganization in adult rat somato- humans the impact of modified use. These studies indicated that sensory cortex (SI). Changes were characterized by a selective parallel to improvement of behavioral performance, extensive enlargement of the cortical territory and of the receptive fields use resulted in substantial changes of cortical representations representing the stimulated skin fields. A control protocol of the (Cohen et al., 1993; Pascual-Leone and Torres, 1993; Elbert et al., identical stimulus pattern applied to only a single skin site evoked 1995; Pantev et al., 1998; Sterr et al., 1998). Although these no changes, indicating that coactivation was essential for induc- studies confirmed the relevance of cortical plasticity for everyday tion. More generally, our protocol offers the advantage to study life, they did not determine the crucial stimulus parameters asso- systematically the impact of input probabilities by variation of the ciated with altered use that lead to the observed reorganization. degree of simultaneity or consistently anticorrelated inputs that is From a number of animal studies, the importance of temporally currently under investigation. correlated inputs and thus the characteristics of the input statis- The selective and local changes within the cortical map implied tics had been hypothesized to play a key role (Clark et al., 1988; that early sensory cortical processing was affected. Only those Fregnac et al., 1988; Allard et al., 1991; Ahissar et al., 1992; areas that underwent a specific alteration in stimulation without Diamond et al., 1993; Wang et al., 1995; Cruikshank and Wein- engaging cognitive factors became reorganized. It is evident, berger, 1996b). In fact, since Hebb (1949), and even since James however, that plastic changes are further subject to modification (1890), the aspect of simultaneity has become a metaphor in via attention, meaning, and reward (Ahissar and Hochstein, 1993; neural plasticity, although the exact role of Hebbian mechanisms Ito et al., 1998; Buchner et al., 1999). in use-dependent plasticity remains controversial (Cruikshank To address the question of how much relevance plastic reorga- and Weinberger, 1996a; Edeline, 1996; Ahissar et al., 1998). nization induced by pure variation of the input statistics (i.e., the temporal and spatial probability distributions of sensory inputs) Received Sept. 16, 1999; revised Nov. 22, 1999; accepted Nov. 30, 1999. has on a perceptual level, we tested the impact of a coactivation We acknowledge support of the Institute for Neuroinformatics (Bochum, Ger- protocol in humans. Assuming that in humans the tactile coacti- many) where the experiments were performed. B.G. was supported by the vation protocol induces equivalent reorganizational processes as Volkswagen-Stiftung Grant AZ I/73035 (junior research group “cortical reorgani- zation and learning”). We thank Dr. Jancke for helpful discussion of this described for rat somatosensory cortex, we expected that discrim- manuscript. ination performance should be subject to modification. The re- Correspondence should be addressed to Dr. Ben Godde, University of Tu¨bingen, sults showed that a few hours of coactivation induced a fast and Institute of Medical Psychology, Gartenstrasse 29, 72074 Tu¨bingen, Germany. E- mail: [email protected]. reversible discrimination improvement as indicated by a lowering Copyright © 2000 Society for Neuroscience 0270-6474/00/201597-08$15.00/0 of the spatial two-point discrimination threshold. 1598 J. Neurosci., February 15, 2000, 20(4):1597–1604 Godde et al. • Plasticity of Discrimination Performance MATERIALS AND METHODS We studied 21 healthy, right-handed subjects (14 male and 7 female) between 22 and 35 years of age in different experimental groups as described below. Because a number of subjects participated more than once, we were able to analyze the data separately with respect to their status as naive or non-naive subjects. Generally, experiments in which non-naive subjects participated were separated by at least 6 weeks. Simultaneous spatial two-point discrimination performance was tested in a two-alternative forced-choice tactile discrimination task. Seven pairs of needles (diameter, 200 ␮m) with separation distances of 0.7, 1.0, 1.3, 1.6, 1.9, 2.2, and 2.5 mm were used. In addition, zero distance was tested with a single needle. The needles were mounted on a rotatable disk that allowed us to switch rapidly between distances. To accomplish a rather uniform and standardized type of stimulation, we installed the disk in front of a plate that was movable up and down. The arm and fingers of the subjects were fixated on the plate, and the subjects were then asked to move the arm down. The down movement was arrested by a stopper at a fixed position above the needles. The test finger was held in a hollow containing a small hole through which the finger came to touch the needles at approximately the same indentations in each trial. Each distance of the needles was tested 10 times in randomized order, result- Figure 1. Learning curves of naive (left) and non-naive (right) subjects. ing in 80 single trials per session. The subject had to decide immediately Thresholds for spatial two-point discrimination as a function of the day of Ϫ whether he or she had the sensation of one or two tips. Generally, the training before induction of changes by a coactivation protocol [day 4 Ϫ index finger of the right hand (right-IF) was tested. The middle finger of (d 4)today0(d0)] are shown. In this and subsequent figures dots the right hand (right-MF) or the index finger of the left hand (left-IF) represent the mean thresholds; horizontal lines within boxes represent the served as a control. medians. Boxes show the top and bottom quartiles, and the outlier caps are The subject’s responses (“0” for one tip and “1” for two tips) were placed on the top and bottom deciles. summed for each distance separately. A sum of 10 indicates that in each of the 10 trials the subject indicated that he or she had perceived two tips. These values were plotted against tip distance as a psychometric function protocol on 3 consecutive days. All data were statistically analyzed using and were fitted by means of a logistic maximum likelihood estimation ANOVA or one-tailed Student’s t test. [adapted from Harvey (1986)]. The threshold was taken from the fitted curve at that distance for which a level of 50% correct responses was reached. RESULTS Experimental testing of the right-IF was performed on 7 consecutive days that were denoted day Ϫ4 to day 2, with day Ϫ4 the first day of the A total of 21 right-handed subjects was tested in a two-alternative test period, day 0 the first day at which the tactile coactivation protocol forced-choice discrimination paradigm to measure simultaneous was applied,
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