Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation

Neuropsvcholo,qia, Vol. 36, No, 4, pp. 363 367, 1998

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Pergamon

PII: S0028 3932(97)00113 9

; 1998 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0028 3932/98 $19.00+0.00

Cortical plasticity in perceptual learning demonstrated by transcranial magnetic stimulation VINCENT WALSH,* ELISABETH ASHBRIDGE and ALAN COWEY Department of Experimental Psychology, University of Oxford, Oxford, UK (Accepted 14 Juh, 1997)

Abstract--Performance on a wide range of perceptual tasks improves with practice. Most accounts of perceptual learning are concerned with changes in neuronal sensitivity or changes in the way a stimulus is represented. Another possibility is that different areas of the brain are involved in performing a task while learning it and after learning it. Here we demonstrate that the right parietal cortex is involved in novel but not learned visual conjunction search. We observed that single pulse transcranial magnetic stimulation (TMS) to the right parietal cortex impairs visual conjunction search when the stimuli are novel and require a serial search strategy, but not once the particular search task has been learned. The effect of TMS returns when a different, novel, serial search task is presented. © 1998 Elsevier Science Ltd. All rights reserved Key Words: perceptual learning; cortical plasticity; visual search: TMS.

Introduction

ner [12]. Further, under most conditions, the effects of training on one kind of visual search task do not transfer to previously unpractised search tasks with new stimuli, i.e. perceptual learning in visual search tends to be both stimulus and task specific [1, 2, 12, 19, 28]. Given the key role of parietal visual areas in conjunction search, the question arises of whether the role changes as one improves on a serial search task and, if so, whether the changes are specific to the training task or generalise to other search tasks. For example, as learning occurs, the neurons activated by the individual features which comprise a stimulus may become more tightly tuned to the relevant stimulus parameters [7, 8, 13] or, alternatively, perhaps new representations of the stimuli are formed in the inferior temporal cortex and the parietal cortex becomes redundant. Alternatively, the neurons involved in a task may simply respond more swiftly or effectively. TMS and an appropriate learning paradigm can be used to distinguish among these possibilities. If it is the case that neurons respond more quickly as learning occurs then the disruptive effects of TMS on visual search should be obtained earlier in a trained than an untrained subject. If new stimulus representations are formed, however, and the strategy the brain uses to solve a learned conjunction task does not involve the parietal cortex, then there might be no effect of TMS over the parietal cortex of a trained subject now performing a conjunction search task preattentively. Here we report that the specificity of learning seen in visual search [1, 2, 12, 19] is reflected in changes

The role of the visual parietal cortex in serial conjunction search has been established in neuropsychological patients [3, 4, l l, 15], in cerebral activation studies using Positron Emission Tomography [10] and with Transcranial Magnetic Stimulation (TMS) [6]. Recent studies of the dynamic nature of the response properties of visual neurons [23, 27] have shown that receptive field profiles may depend on context and experience, making it unlikely that the contribution of any visual area to a particular task will be hard-wired. In the specific case of visual search, for example, one would expect that as performance on search tasks undergoes training so the regions of cortex involved in the tasks would reflect that learning in changes in their relative contributions to performance. In a previous paper [6] we demonstrated that TMS applied to the right parietal cortex produces an impairment in a serial but not a parallel visual search task. Of course, performance on visual search tasks is not static, it improves with practice [1, 2, 12, 19] and tasks which were initially performed using a serial strategy can eventually come to be performed in a pre-attentive man-

* Address for correspondence: Department of Experimental Psychology, Oxford University, South Parks Rd, Oxford OXI 3UD, UK; e-mail: vin(~psy.ox.ac.uk. 363

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in the effects o f T M S over the p a r i e t a l cortex: new visual c o n j u n c t i o n searches are i m p e d e d by T M S , highly p r a c tised c o n j u n c t i o n search i s not. S o m e o f these d a t a have been r e p o r t e d at a recent conference [5].

Methods

TMS equipment Full details of the stimulator are given in our previous report [6]. Briefly, the stimulator was a MagStimTM Model 200 (maximum output 2 T). Stimulation was applied at 80% of the maximum using a figure-of-eight 70 mm coil with which good spatial resolution (approx. 1 cm) can be obtained [17, 21].

Subjects Three subjects took part in both the learning and transfer of two conjunction search tasks. The subjects had taken part in our earlier experiment which demonstrated that TMS over right parietal cortex disrupted serial search. All were right handed, had normal vision and with one exception were naive to visual search before the experiment. All subjects gave informed written consent and reported absence of epilepsy, or any other neurological condition in themselves and their known family history. Local ethical committee approval was granted 'for all procedures.

Stimuli We used two arrays to assess the effects of TMS on visual search One array (which we shall call the training array) presented a conjunction search in which the target was a green vertical bar and the distractors were green horizontal and blue vertical bars (i.e. the target is defined by a conjunction of orientation and colour). In the transfer experiment, the array (which we call the tr'ansfer array) presented a purple, square target and non-targets were pink squares and purple circles. Stimuli were presented on a 270 x 200 mm PC monitor at a distance of 100 cm from the observer, whose head was stabilised with a chin rest and head strap. The screen was divided into an 8 column x 6 row array of 48 virtual boxes and on any trial each target or distractor could appear randomly in any one of 36 of these boxes. Presentation was not restricted to a single hemifield. The 36 boxes in which the stimuli could appear were the three most lateral columns in each half of the screen. The stimuli were therefore always presented a minimum of 3.16 degrees lateral to the central fixation spot. The background was always black. The bars in the training array subtended approximately 1.1 x 0.2 degrees of visual angle, the squares and circles in the transfer array had diameter/side of 1.1 degrees. T o p r e v e n t unwanted alignment of the stimuli in the arrays they were randomly displaced by +0.3 degrees in horizontal and/or vertical directions. Subjects were required to report the presence/absence of a target by pressing one of two mouse buttons. Speed and accuracy were stressed in the instructions to the subjects. In the TMS stimulation conditions only one set-size (eight) was used [6]. The target was present on 50% of trials. On each trial the subject was presented with a 500 msec alerting tone and a fixation spot in the centre of the monitor. The fixation spot disappeared at the end of the tone. The search array was presented for a maximum of 750 msecs or until the subject made a response. lntertrial interval was 4 secs. This is longer than is usually used

in search experiments and was determined by the recharging requirements of the stimulator [7].

Strategy Baseline measures. We obtained baseline reaction times (RT) on the search tasks to establish the parallel/serial nature of the search. The subjects performed 100 trials on each task with set sizes of three, eight and 16 stimuli. Two stages of experimentation then followed. Stage 1: training. The subjects trained on the conjunction training array for 500 trials per day (mean 2500 trials per subject), without TMS, until their performance became parallel, i.e. R T x set size slope was less than 10msecs per item. At the end of this training phase the subjects received TMS according to the protocol outlined below. They then went on to Stage 2. Stage 2: transfer. The subjects were introduced to the transfer array, the previously unseen visual conjunction of shape and colour and they underwent TMS as for Stage 1 with the differences described below.

TMS protocol The stimulation site used was the one that had proved most effective with the subjects in a previous experiment [6], over the parietal lobe of the right hemisphere. Subjects received 150 trials with stimulation being delivered at array onset-pulse onset asynchronies of 0, 20, 40, 60, 80, 100, 120, 140, 160, 180 or 200msecs after stimulus presentation. Trials were given in blocks of 75 trials and each block was followed by 40 trials in which no TMS was delivered. More TMS than none TMS trials were required to ensure that TMS occurred often enough at all SOAs. In the transfer condition, additional stimulation times up to 280 msecs post stimulus onset were included because in pilot studies the shape/colour conjunction task had proved more difficult for some subjects than the orientation/colour.

Results

Baseline measures T h e c o n j u n c t i o n searches yielded slopes for R T x set size characteristic o f serial search (greater t h a n 10 msecs p e r i t e m a n d an a b s e n t / p r e s e n t slope ratio a p p r o a c h i n g 2:1). T h e training task h a d initial slopes o f 15.8 a n d 24.15 msecs p e r item for target present a n d a b s e n t trials respectively. F o l l o w i n g training, the c o r r e s p o n d i n g figures were 6.69 a n d 8.05 msecs per item. The baseline times o f present a n d a b s e n t trials for the transfer task were 11 a n d 21.5 msecs p e r item.

Training task F i g u r e 1 shows the effects o f T M S on the training t a s k before training t o o k place (i.e. when search was serial). There was significant elevation in reaction times when the pulse was a p p l i e d either 100 msecs ( p < .05 on target present trials) or 160 msecs (p < .05 on target a b s e n t trials) after stimulus onset. F o l l o w i n g training, however, when

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Fig. 1. The effects of TMS on unlearned visual search with eight stimuli in the training array, normalised to the reaction time on trials when search was performed without TMS. There is a clear effect of TMS on trials when the target was present if the pulse was delivered 100 msecs after stimulus onset (p < .05) and also when the target was absent if the pulse was delivered 160 msecs (p <.05) after target onset. Solid lines, target present; broken lines, target absent. Vertical bars represent _ 1 standard error.

performance was parallel, there were no significant effects of TMS on search rates (Fig. 2) when the pulse was applied at exactly the same location as that which yielded the data shown in Fig. 1. Comparison of Figs 1 and 2 also shows that before training there was a residual effect of TMS at times other than 100 and 160msecs after stimulus onset, and that this disappears after training. Transfer task. Figure 3 shows that the effect of TMS returns when a novel search task is used. The effects occurred for this particular shape × colour conjunction task when TMS was applied at 160msecs (p<.05 on target present trials) and 240msecs (p<.05 on target absent trials) after stimulus onset. Note also that the slight effects at other times, which were observed before (Fig. 1) but not after (Fig. 2) training. Discussion The ineffectiveness of TMS following training suggests that right parietal cortical mechanisms are no longer

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Fig. 2. Following several days of training (mean 2500 trials per subject) subjects again received TMS over right parietal cortex. TMS no longer elevated RTs at any of the stimulation times. Solid lines, target present; broken lines, target absent. Vertical bars represent + 1 standard error.

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Fig. 3. The specificity of learning is reflected in the specificity of TMS effects. Whereas TMS over parietal cortex during performance of the task on which learning had occurred yielded no effects, TMS during performance of the novel search again slows performance when applied 160 msecs after onset of the array (p <.05) on target present trials and 240 msecs (p <.05) after onset on target absent trials. Vertical bars represent + 1 standard error.

necessary for conjunction visual search once the task can be performed in parallel. If so, TMS with a fresh visual search task which required serial search should reinstate the effect. As expected, because perceptual learning in visual search can be stimulus specific [1, 2, 12, 19], this new conjunction task was performed as a serial search, with slopes of greater than 10msecs per item and an absent/present slope ratio approaching 2:1. The relative difficulty of the two conjunction tasks observed in pilot trials was not sustained in the experiment, raising the possibility that some learning had transferred. However, because the critical TMS times in the transfer task (Fig. 3) were later than in the train&9 task (Fig. 1) it seems more likely that subjects had improved on aspects of the task other than sensory (e.g. motor or decision making components of search). It is important to note that in the transfer task, as in the training task, the order of TMS effects are in line with reaction times---faster (target present) RTs are associated with an early critical time for the effect of TMS relative to slower (target absent) RTs. Consistent with other evidence [3-6, 15, 16, 22], our finding demonstrates the importance of right parietal visual cortex for attentive but not pre-attentive visual processes. We can be sure the lack of TMS effect after training is not due to a general elevation of the threshold for disrupting the neural circuits involved in search; if this were the case, there would not have been an effect of TMS on the new task. In addition, the result shows that the involvement or indispensable role of the parietal cortex diminishes with practice but that this change is limited to the particular visual conjunction used rather than to conjunction search in general [12, 19, 28]. Does this changing role of parietal cortex reflect improvements/changes in the functions carried out by other brain regions (for example, areas in the temporal visual stream have some capacities for spatial attention, see Ref. [19]), or the devel-

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opment of new feature templates in temporal cortex that allow a conjunction target to become like a single popout feature in a visual search task (see Ref. [8])? If changes due to visual perceptual learning are independent of stimulus parameters they should generalise across other search tasks: they don't [1, 2, 7, 12 14, 18, 19, 24-26, 30]. Nor can one explain the effect in terms of improved efficiency of the parietal cortex since this should result not only in transfer across tasks but also to a reduction in the time at which TMS is effective. The most plausible explanation, then, lies in modifications in the responsiveness of temporal lobe visual neurons, which may form a new feature template upon repeated presentations of a target and its distractors (see Ref. [29]). These new templates would enable a search that was previously serial to become parallel and therefore would not require attentional engagement and feature binding mediated by the parietal cortex. A similar explanation based on Guided Search [31] would be that learning occurred as an increase in the efficiency of the separate channels activated in parallel by colour and orientation. We have concentrated on the times at which we observe large effects of TMS. However, it is clear from Fig. 1 that there are small, residual effects at several other times. These residual effects disappear following training (Fig. 2) and reappear when subjects are presented with a new task (Fig. 3). Perhaps these residual effects should serve as a warning against looking for 'magic times' at which the parietal cortex becomes important for a task. If the parietal areas are important for feature binding it seems reasonable to argue that there would be constant interaction between the parietal regions and the extrastriate areas responsible for analysing information about colour and form. The residual effects, then, may be interpreted as evidence of disrupting the interaction between different cortical regions, whereas the peak effects reflect disruption of the outcome of the interaction between these regions. This evidence for plasticity in the role of parietal cortex in visual search opens up several new possibilities for understanding changes in how a task is performed with practice. With TMS in particular it will be possible to examine the role of parietal cortex in early and late components of learning [18], to look at the time course of activity as a function of the different numbers of distractors and to assess the predictions made by different models of visual search.

Note added in proof

Following these experiments we investigated two other forms of transfer. Following training on the first conjunction task (green vertical from green horizontals and blue verticals) two subjects were tested for transfer and TMS effects with the same stimuli presented at twice the distance (i.e. half retinal image size) and also with new conjunctions of the same colour/orientation elements the

(blue horizontal as the target and green horizontal and blue vertical as distractors). Unlike learning with popout arrays full transfer of learning was observed in the distance condition (i.e. the task was performed in parallel) and TMS did not affect RTs. Intriguingly, in the reverse stimuli condition, one subject transferred (i.e. maintained parallel search) but one reverted to serial search. The effects of TMS reflected these individual differences: the subject who transferred was unimpaired by TMS whereas an effect of TMS returned in the subject who reverted to serial search.

Acknowledgements--This work was supported by an MRC Program Grant, by a grant from the EC Human Capital and Mobility Program and by a McDonnel-Pew Centre for Cognitive Neuroscience in Oxford Research Fellowship awarded to E.A. We are grateful to Dr M. Rushworth for reading the manuscript and for his assistance with calculation and calibration of magnetic fields. We thank an anonymous referee for bringing to our attention the disappearance and reappearance of residual effects of TMS at times other than those at which we observe main effects.

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