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Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus

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Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus Katrina Carlsson, Predrag Petrovic, Stefan Skare, Karl Magnus Petersson, and Martin Ingvar Karolinska Institute/Karolinska Hospital, Sweden Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/4/691/1758760/089892900562318.pdf by guest on 18 May 2021 Abstract & Predictions of the near future can optimize the accuracy during both states included the contralateral primary sensory and speed of sensory processing as well as of behavioral cortex, bilateral areas in the inferior parietal lobules, the responses. Previous experience and contextual cues are putative area SII, the right anterior cingulate cortexand essential elements in the generation of a subjective predic- areas in the right prefrontal cortex. Similarly, common tion. Using a blocked fMRI paradigm, we investigated the decreases were observed in areas of sensorimotor cortex pattern of neural activation in anticipation of a sensory located outside the area representing the target of stimulus, stimulus and during the processing of the somatosensory i.e., areas that process information which is irrelevant to the stimulus itself. Tickling was chosen as the somatosensory attended process. The overlapping pattern of change, during stimulus rather than simple touch in order to increase the the somatosensory stimulation and the anticipation, furthers probability to get a high degree of anticipation. The location the idea that predictions are subserved by a neuronal and nature of the stimulus were well defined to the subject. network similar to that which subserves the processing of The state of anticipation was initiated by attributing an actual sensory input. Moreover, this study indicates that uncertainty regarding the time of stimulus onset. The activation of primary somatosensory cortexcan be obtained network of activation and deactivation during anticipation without intra-modal sensory input. These findings suggest of the expected stimulus was similar to that engaged during that anticipation may invoke a tonic top-down regulation of the actual sensory stimulation. The areas that were activated neural activity. & INTRODUCTION & Petersen, 1990). Hence, anticipation allows for The human capacity to perform real time information more pertinent reactions in the immediate situation processing is limited. The limited speed of neuronal (James, 1890). operations may partly be compensated for by parallel A high-quality prediction in the somatosensory do- interactive and distributed processing (Rumelhart & main carries defined information, not only on what or McClelland, 1986). Another mechanism may be the where something is going to happen, but also when it transformation of initially controlled processing to- will happen. The most accurate predictions can be wards automaticity. Automaticity implies a gain of made when the input represents sensory feedback speed and precision at the possible cost of flexibility from self-generated actions since this implies precise (Schnieder & Shiffrin, 1977). It also implies a de- information on all aspects including the time domain of creased computational demand, which in turn im- the coming event (Blakemore, Wolpert & Frith, 1999; proves the capacity for simultaneous processing. An Blakemore, Wolpert, & Frith, 1998). The predictions alternative way of increasing the efficiency of informa- become more uncertain when they are applied to tion processing is to continuously update predictions externally generated sensory input. Previously acquired of what is to be expected. Explicit or implicit predic- knowledge, combined with presently available contex- tions allow for selective and focussed processing of tual information from different sensory modalities may sensory input (Corbetta, Miezin, Dobmeyer, Shulman, then be used to generate predictions. For example, a & Petersen, 1991; Posner & Petersen, 1990) as well as prediction of the tactile aspects of a planned touch of a detailed planning of behavior and a reduction of the surface may be made from visual input in combination number of options in the behavioral repertoire with experience. A manipulation of the degree of (Broadbent, 1958). If a subject is able to make predictability of an event provides an opportunity to accurate predictions, the time and accuracy of re- study anticipatory mechanisms in the brain (Hsieh, sponses at the behavioral level are improved (Posner Stone-Elander, & Ingvar, 1999). D 2000 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 12:4, pp. 691±703 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892900562318 by guest on 02 October 2021 Conceptually, relevant predictions may serve as a tickled the subjects with a light touch of painter's brush guide for attention. In experimental settings, it has been on the foot sole. A similarity between the patterns of shown that attention mechanisms may modulate the response during anticipation and tickling would further activity in lower order sensory cortices (Frith & Dolan, the idea that predictions are subserved by a similar 1997; Drevets et al., 1995; Corbetta et al., 1991). In the neuronal network as that which subserves the proces- study by Drevets et al. (1995), the subjects were asked to sing of actual sensory input. We used functional mag- count infrequent touches with von Frey's hair or antici- netic resonance imaging (fMRI) to monitor the pate a painful stimulus. That PET study showed de- functional activity during anticipation of a well-defined creased neural activity in the parts of the primary somatosensory stimulus as well as during the sensory sensory cortexthat were outside the area representing stimulus itself. The anticipatory state was elicited with a Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/12/4/691/1758760/089892900562318.pdf by guest on 18 May 2021 the skin locus of the expected stimuli. In an earlier 2-D visual cue that carried information of a change in context rCBF 133Xe study, with a similar task of counting infre- and thereby indicated when the subject should antici- quent light touches, increased neural activity was re- pate a sensory stimulus. ported in an area of primary sensory cortexdefined as representing the target of stimulation (Roland, 1981). In RESULTS spite of the apparent inconsistency between those re- sults, possibly due to methodological differences, they All subjects withstood the sessions in the camera well both point to the possible existence of an attentional and none complained of discomfort. Before entering the modulation during anticipation. The attentional me- camera, the subjects rated their level of ticklishness, The chanism for such a modulation of neural activity in the self-reported estimation was 66 6 (mean SEM)on absence of stimulus presentation can be described in the VAS scale (0±100, not at all ticklishÐmore ticklish terms of a bias signal (Rees & Frith, 1998). A bias signal than anyone I know). The subjects estimated the mean would improve the computational efficiency in the area tickling sensation in the experimental situation to be 50 of interest and suppress responses outside the focus of 6 (0±100, no experience of tickleÐmaximally imagin- attention (Ghatan, Hsieh, Petersson, Stone-Elander, & able level of tickling) and the desire to move during Ingvar, 1998). Modulations of relevant low level proces- tickle to 40 8 (0±100, no desire to moveÐirresistible sing areas without external input have also been illu- desire to move). None of the subjects described the strated in motor and sensory imagery studies, i.e., in a tickling as unpleasant. All subjects associated the red situation when the subject is imagining the stimulus, but color square with tickling, described increased alertness not expecting a real stimulus in the near future (Hodge, when it was displayed, and acknowledged a sense of Dubroff, Huckins, & Szeverenyi, 1998; Kosslyn, Thomp- anticipation during the runs when the red square was son, & Alpert, 1997; Roth et al., 1996). The activation of shown with no tickling. In four out of seven cases, the the same neural network during imagery as that which is sense of anticipation was reported as a marked phenom- responsible for the actual movement or sensation is enon. The sensation of tickle was perceived as more consistent with the suggestion by James (1890) that intense at the end of each tickling epoch (4/7 cases). ``sensation and imagination are due to the activity of the same centers in the cortex.'' Sensory Stimulation Compared to Rest The underlying hypothesis for the present work is (SS versus RS) that a prediction of an external event is a cerebral mechanism that serves to optimize the accuracy and Maximum Z scores for MRI signal change in the sensory speed of sensory perception. Based on earlier imaging stimulation state versus rest are listed in Table 1A. data (e.g., Drevets et al., 1995; Roland, 1981) we de- Activated areas in the right frontal lobe, ipsilateral to signed an experiment to test the hypothesis that neuro- the stimuli, included parts of orbitofrontal and lateral nal computations may precede the actual response or frontal cortex(Broddman's area (BA) 10, 44, 47 and 49) behavior. Specifically, we wanted to test if the neural as well as the anterior cingulate (ACC, BA 32). In the left response in anticipation of a sensory input is similar to frontal lobe, the activations were restricted to BA 44. the response to the actual sensory input. Tickle is Increases were also observed
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