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Attention to somatosensory events is directly linked to the preparation for action
Journal of the Neurological Sciences 279 (2009) 93–98
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Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Attention to somatosensory events is directly linked to the preparation for action Imke Galazky a,⁎, Hartmut Schütze a,b, Toemme Noesselt a, Jens-Max Hopf a,c, Hans-Jochen Heinze a,c, Mircea Ariel Schoenfeld a,c,d a
Department of Neurology, Otto-von-Guericke University Magdeburg, Germany Department of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, Germany Leibniz Institute for Neurobiology Magdeburg, Germany d Kliniken Schmieder, Allensbach, Germany b c
a r t i c l e
i n f o
Article history: Received 29 April 2008 Received in revised form 1 December 2008 Accepted 3 December 2008 Available online 23 January 2009 Keywords: Somatosensory system Attention to touch fMRI Preparation for action
a b s t r a c t The present study investigated the neural basis of attention in the somato-sensory system. Subjects directed their attention towards their left or right hand while functional MRI data was collected during tactile stimulation of the fingers. Activations evoked by tactile stimuli when a stimulated hand was attended vs. unattended were contrasted. The tactile stimuli elicited hemodynamic responses in the contralateral primary and secondary somatosensory cortex. No attentional modulations of the BOLD-response could be observed in these regions. However, attention-related modulations were observed at more anterior locations in the ipsiand contralateral primary motor cortex and in the supplementary motor area. This pattern of results suggests, that attention to somato-sensory events is directly linked to the motor system and the preparation for action. This mechanism appears to be in stark contrast to visual or auditory attention, which primarily serve to separate relevant from irrelevant information. © 2008 Elsevier B.V. All rights reserved.
1. Introduction From the early days of neuroimaging the somato-sensory system has been subject to extensive research. While the pioneering work mainly employed electrophysiological measures of brain activity now, recently developed methods like functional magnetic resonance imaging (fMRI) offer the possibility of investigating this system in humans with a high spatial resolution. Investigations of the topographical distribution of the activated brain regions can complement the large body of available electrophysiological data and lead towards a deeper understanding of physiological processes. It should be noted that, so far, both hemodynamic and electrophysiological approaches have provided converging evidence on the somatotopic functional organization of the somatosensory cortex, confirming the long-standing knowledge on the “homunculus” in the primary somato-sensory cortex [1]. One of the key questions in the research on sensory systems concerns the role of attention. In the visual and the auditory system attention has been shown to play an eminent role by ‘filtering out’ unwanted information and by enhancing relevant information. These mechanisms enable our brain to deal with the massive input constantly bombarding those sensory systems. Several mechanisms for accomplishing this have been described, some working by enhancing the gain of the wanted information [2–4], other by
⁎ Corresponding author. E-mail address: [email protected] (I. Galazky). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.12.006
suppressing unwanted information [5,6]. Both of these mechanisms might also operate at the same time [7]. It is important to note that these attentional mechanisms operate in those regions in which the sensory processing of the perceived features takes place [8]. A key question, however, concerns the exact level of processing at which the attentional modulations occur. Lately, in the visual system, a growing body of evidence has emerged indicating that the primary visual cortex (area V1) is indeed subject to attentional modulations (reviewed in [9]). While it is currently under discussion whether these modulations in V1 occur during or after the initial flow of activity, there is now no doubt about the fact that activity in area V1 is modulated by attention [10,11]. The picture is less clear for the primary somato-sensory cortex. Animal studies have shown that attention can facilitate [12] but also suppress [13] stimulus processing in this region. Other studies have reported that tactile stimuli are effectively processed regardless whether they are attended or not [14–16]. Nevertheless, there is some evidence that primary and secondary somato-sensory areas might be subject to attentional modulation in humans. Data bearing on this have been provided by somato-sensory evoked potentials (SEP), magnetoencephalography (MEG), positron emission tomography (PET), and fMRI studies [17–29]. While some studies have reported attentional modulations in the primary somato-sensory cortex (S1) using different methodologies [23,26,30], other studies have mainly found activation changes in the secondary somatosensory cortex (S2) [19,29]. Other studies have shown increased activations in both S1 and S2 [27,31] or no difference in the attentional
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modulation between S1 and S2 at all [18]. In general, most of the previous fMRI studies have either found attentional modulations in areas S1 or S2 to be quite small or not present at all [17]. A key question is what aspects of the different studies might have led to the different and in part conflicting results. A close look at the employed experimental designs suggests two important considerations that are germane to this issue. Whenever activity has been found in the primary somato-sensory cortex, it has been rather small in magnitude. Secondly, the likelihood of detecting attentional modulation in this region appears to strongly depend on the choice of the control task. The studies that found such modulations in the primary sensory cortex employed designs in which tactile stimuli had to be actively suppressed in the unattended (control) condition (reviewed in [17]). This observation suggests that the observed modulations in the primary somato-sensory cortex in the attention vs. control contrasts stem from suppression in the unattended control condition rather than from enhanced processing in the attend condition. In order to investigate whether this is indeed the case, we chose a paradigm in which attention is directed towards and away from identical physical stimuli, thereby attempting to avoid sensory confounds. We chose to use a block design because the results would typically be very robust. While tactile stimuli were delivered to fingers II and V of both hands, attention was directed towards or away from one hand, by asking the subjects to either count the stimuli delivered to that hand or those delivered to the other hand. In this way it was possible to compare the activity elicited by exactly the same tactile event (e.g. stimuli delivered to the left index finger) while the left hand was attended (the attended condition for left hand) and while the right hand was attended (the unattended condition for left hand). Since the subject is counting in both cases and the physical stimuli are identical, putative differences in fMRI activity can only be related to the different attention conditions. In contrast to other sensory systems the importance of attention to touch appears to be rather small in humans. Evolutionary and cultural factors like the wearing of clothes have rather made it necessary to suppress input from skin sensors, than enhance their processing. In contrast to many animals, where somato-sensory events are an important alarming signal, there is no essential need to sort out relevant from irrelevant tactile events in humans. This is in line with the findings of most previous studies, in which attentional modulations in the primary somato-sensory cortex were rather small and in most cases only present when stimuli had to be either ignored or actively suppressed in the control task [17]. Consequently, we speculated that in the present study attentional modulations would be rather small in the primary somatosensory cortex and more pronounced in brain regions related to alertness and motor planning. 2. Methods 2.1. Subjects The ethics committee of the University of Magdeburg approved the study. After giving informed consent, fifteen young healthy subjects participated as paid volunteers in this study: nine were women and six were men, mean age 24 years (SD 3, 8, range 22–37). All subjects were right handed.
scanning the pneumatic devices at the fingertips were adjusted until the subject reported equal stimulation intensity at all four stimulation sites. The timing was controlled by a microcomputer and the experiment consisted of four experimental runs of 8 min each. Consequently, each finger (stimulation site) received three blocks of stimulation during an 8 min run. The sequential order of the stimulation sites (blocks) was pseudo-randomized. Before the run started the subjects were verbally instructed to pay attention to one hand (left or right) and to count in mind the stimuli delivered to the fingers of that hand. Stimuli delivered to the other hand were to be ignored during that run. The left and right hand attention conditions were counterbalanced across the four runs. After each run the subjects reported the count of delivered stimuli for each finger of the attended hand. 2.3. MRI data acquisition 2.3.1. fMRI The subjects were scanned in a 1.5 Tesla scanner (General Electric Signa Horizon LX, neuro-optimized, General Electric Inc., Milwaukee, WI, USA) with a standard GE headcoil. The functional images were acquired using a gradient echo single shot echo-planar-imaging (EPI) sequence with time of echo (TE)/time of repetition (TR)/bandwidth/ flip angle = 40 ms/2 s/83 kHz/80°. Twenty-three slices (5 mm thickness, 1 mm gap, field of view 200 mm, matrix 64 × 64) parallel to the anterior–posterior commissure line, covering the full brain were acquired. In each functional run 240 volumes were collected resulting in a scan time of 8 min per run. 2.3.2. Anatomical images Structural MRI was performed in a separate session. A T1-wheigted high resolution data set was acquired using a three dimensional single pulse gradient recovery sequence with TE/TR/flip angle = 8 ms/24 ms/ 30°. In each functional session a T1-weighted EPI (Inversion recovery prepared EPI, TE/TR/time of inversion = 16 ms/12 s/1050 ms) image set was collected with slice parameters identical to the functional data. 2.4. MRI data analysis The MRI data were analyzed using SPM2 (Wellcome Department of Cognitive Neurology). The recorded data were analyzed with the preprocessing routines provided by the package, including realignment, co-registration and spatial normalization to the MNI template. The statistical analyses were carried out on smoothed (8 mm fullwidth Gaussian kernel) images. Two types of comparisons were performed. In order to assess the effect of tactile stimulation, blocks with tactile stimulation delivered to the unattended hand were contrasted with the rest periods for each of the four sites. The effect of attention was revealed contrasting stimulation periods at exactly the same stimulation site (for example the right index finger), when the hand was attended (i.e. subjects counted the number of stimuli delivered to the right hand) vs. unattended (i.e. subjects counted the number of delivered stimuli to the left hand). It is important to note that in these types of comparisons the physical stimulus is always identical (e.g. 20 s tactile stimulation with a pace of 1 Hz delivered to the same fingertip), while attention is manipulated towards and away from the respective hand. A random effects model was employed to perform the group analysis.
2.2. Experimental paradigm 3. Results Subjects were presented with a classical fMRI block design paradigm, consisting of alternating stimulation and pause periods with duration of 20 s each (see Fig. 1). During stimulation blocks tactile stimuli were applied to either the index finger [D2] or to the fifth finger [D5] of the left or the right hand, with a frequency of 1 Hz. The stimuli were delivered using a custom made pneumatic device via plastic tubes carrying compressed air to synthetic membranes taped to the fingertips. Before
3.1. Behavioral results Overall, the subjects made few errors in counting and reporting the correct number of tactile stimuli, with a 96.2% accuracy rate. No significant differences in accuracy were observed between left (97%) and right (95.4%) hand counts F(1,14) = 1.46; p N 0.05.
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Fig. 1. The figure shows a typical experimental run. Subjects were presented with alternating periods of stimulation and rest with duration of 20 s each. Tactile stimuli were applied block-wise to the right index finger [d2r], the right fifth finger [d5r], the left index finger [d2l], and the left fifth finger [d5l] with a frequency of 1 Hz. The experiment was carried out in four experimental runs with a duration of 8 min each. Prior to each run the subjects were instructed to count in mind the stimuli delivered to either the fingers of the right or the left hand. After each run the subjects reported the count of delivered stimuli for each finger of the attended hand.
3.2. Sensory responses to tactile stimulation The activity elicited by tactile stimulation was assessed by comparing blocks of tactile stimulation in unattended conditions vs. the rest periods with no tactile stimulation separately for the left and right hand. Stimulation led to activations of the primary (S1) and secondary (S2) somato-sensory cortex in the contra-lateral hemisphere and in the cingulate gyrus (see Fig. 2). In detail, tactile stimulation of the right fingers elicited activations of the left postcentral gyrus (MNI-coordinates −48/−28/60), the left transverse temporal gyrus (MNI −40/−20/20) and the cingulate gyrus (MNI 0/0/ 40). During tactile stimulation of the left fingers we found activations of the right postcentral gyrus (MNI 44/−24/60), the right lateral sulcus (MNI 40/−20/16) and the cingulate gyrus (MNI 0/−4/40). In both hemispheres clusters of activation during tactile stimulation of the fifth fingers (right D5: MNI −52/−28/48, left D5: MNI 40/−35/54) were localized laterally and posterior to those hemodynamic responses evoked by identical stimulation of the index fingers (right D2: MNI −52/−24/56, left D2: MNI 42/−24/60) (see Fig. 3). 3.3. Attentional modulations In the attention condition tactile stimulation also elicited hemodynamic activity in the contralateral primary somato-sensory cortex (S1), the contralateral secondary somato-sensory cortex (S2) and the cingulate cortex. In addition activation was observed in the supplementary motor area (SMA). Compared to the locations of the activations during tactile stimulation in the absence of attention the attention-related activations were found to be located more laterally and anterior. To investigate which areas are modulated by attention the responses to the identical tactile stimuli in the attended conditions were contrasted with those in unattended conditions. These contrasts revealed activations located in the precentral gyrus in both the
contralateral and ipsilateral hemisphere as well as in the SMA (Fig. 4), but not in the postcentral somatosensory areas. Attention to tactile stimulation of the right fingers elicited hemodynamic responses in the left (MNI −56/−4/44) as well as in the right precentral gyrus (MNI 56/ −4/40) and in the medial frontal gyrus (MNI −4/−8/60). Attention to left hand stimuli led to activations in the right (MNI 56/−4/48) and left precentral gyrus (MNI −52/−8/44) and in the medial frontal gyrus (MNI −4/−4/68). Table 1 shows the reported activations for those conditions. 4. General summary The somato-sensory stimulation elicited activity in the contralateral S1, with a topographical distribution corresponding to the well known homunculus [1]. Additional activity was observed in an area within the cingulate gyrus, which has previously been described to reflect subjective aspects of the stimulation [39]. Importantly, the locations of the attentional modulations did not match the locations of the regions activated in the primary somato-sensory cortex (S1) during tactile stimulation. The revealed attention-related clusters of activation were localized more laterally and anterior (see Fig. 3). Visual inspection and Talairach co-ordinates identified these regions as the primary motor cortex (M1) in the ipsilateral and contralateral hemisphere. In addition to the bilateral primary motor cortex activations, attention related modulations were also observed in the supplementary motor area (SMA). 5. Discussion In the present study, we investigated the neural correlates of attention to tactile stimuli delivered to the index (D2) and little finger (D5) of the left and right hand under attended and unattended conditions. Unattended tactile stimuli elicited hemodynamic activity in the contralateral primary (S1) and secondary somato-sensory
Fig. 2. Group analysis: The figure shows the regions activated during tactile stimulation (red colour: activations during left side stimulation; blue colour: activations during right side stimulation, both contrasted vs. the rest condition) (see also Table 1) across the subjects. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
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Fig. 3. Group analysis: The figure shows the spatial distribution of activations by tactile stimulation of the index finger (red colour) and fifth finger (blue colour) for both hemispheres across the subjects. Note the somatotopic topographical distribution. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
cortex (S2), as well as in the cingulate gyrus (see Fig. 2). The activations in S1 in response to contralateral stimulation delivered to D2 and D5 had slightly different locations, corresponding to the somatotopic organization of this region (the response to D5 stimulation was more lateral and posterior compared to D2 stimulation, see Fig. 3). The location of the activations are fully consistent with findings from electrophysiological recordings (SEP [21–23] and MEG [24,25]). Importantly, when attention was directed to the corresponding hand where the stimuli were delivered, no significant modulations could be observed in S1. An enhancement of activity was observed in regions located more anterior, namely in the primary motor cortex (M1) and in the supplementary motor area (SMA) (see Fig. 4). The modulations in area M1 were observed in both, the ipsilateral and the contralateral hemisphere to the delivered tactile stimulus. These results show that attention to tactile stimuli primarily modulates hemodynamic activity in motor areas, suggesting that this type of attention might be directly involved in the preparation for motor action. Previous studies investigated changes of neuronal activity in the somatosensory cortex under conditions when tactile stimuli were attended vs. unattended. Modulations of activity have been reported using a variety of methods like single unit recordings in monkeys [32,33], SEPs [21–23], MEG [24,25], PET [26–28] and fMRI [17–20,29] in humans. Nevertheless, important questions remained with respect to both the nature of the modulations and their functional role. While enhancement of activity in the primary somato-sensory cortex (S1) has been reported in some fMRI studies [23,30], others have showed decreased activity in areas other than S1 [26], or no modulation at all [18] when using conventional group analysis approaches. A similar puzzle emerges from the findings with regard to the secondary somatosensory cortex (S2). Backes et al. [19] and Staines et al. [29] showed an increased BOLD response in the secondary somato-sensory cortex for
attended vs. unattended somato-sensory stimulation. Other authors reported a simultaneous increase of activations in S1 and S2 [27] or a greater increase in S2 than S1 [34]. However, there are also reports of no difference at all in the attentional modulation between S1 and S2 [18]. In the present study attentional modulation was neither found in the primary (S1) nor in the secondary (S2) somato-sensory cortex. This somewhat surprising result is probably due to the fact that we used a conservative group analysis approach. The small physical size of the effects in these regions paired with inter-individual variability apparently make it difficult to detect changes due to attention at group level [17]. This result replicates the findings of Johansen-Berg et al. [18], who also did not find attentional modulations in S1 or S2 at group level. Nevertheless, this does not mean that S1 or S2 are not modulated at all by attention. Johansen-Berg et al. [18] for example performed a region of interest analysis on their data and were able to find small attentional modulations that were not revealed by the previously performed group analysis. In addition, most of the previous studies reporting attentional modulations in S1 and S2 employed paradigms in which attention was actively withdrawn by distraction in the unattended condition to maximize the effect [20,28] (reviewed in [17]). This is very different from the paradigm used here. It should be kept in mind that the task difficulty in the present experiment was rather low, as indicated by the high accuracy rates in the behavioral data. Consequently, under low attentional load S1 and S2 do not appear to be strongly modulated by attention. S1 and S2 might well be modulated by attention when the task difficulty is increased, or when the allocation of resources is higher due to high attentional load. In addition, the well-known right hemispheric dominance for attentional processing could have contributed to the lack of attentional modulation in S1 found here. Another potential confound arises from the left hemispheric specialization for counting. Often numbers are verbalized or fingers are imagined during counting.
Table 1 Activations for attended and non-attended condition during tactile stimulation of the right and left fingers Condition Non-attended stimulation of the right fingers
Non-attended stimulation of the left fingers
Attended stimulation of the right fingers
Attended stimulation of the left fingers
Anatomical regions Postcentral gyrus Transversal temporal gyrus Cingulate gyrus Postcentral gyrus Lateral cerebral sulcus Cingulate gyrus Contralateral precentral gyrus Ipsilateral precentral gyrus Supplementary motor area Contralateral Precentral gyrus Ipsilateral precentral gyrus Supplementary motor area
Functional description
x
MNI coordinates y
z
S1 S2 – S1 S2 – M1 M1 SMA M1 M1 SMA
−48 −40 0 44 40 0 −56 56 −4 56 −52 −4
−28 −20 0 −24 −20 −4 −4 −4 −8 −4 −8 −8
60 20 40 60 16 40 44 40 60 48 44 68
k
pcorr
18 10 2 61 30 84 72 13 93 5 10 18
0.042 0.001 0.001 0.0001 0.006 0.0001 0.010 0.010 0.013 0.010 0.010 0.053
S1—Primary somatosensory cortex, S2—Secondary somatosensory cortex, SMA—Supplementary motor area, k—number of activated voxels, pcorr—corrected probability for multiple comparisons.
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Fig. 4. Group analysis. The figure shows the spatial distribution of activation patterns elicited by contralateral (unattended) tactile stimulation (in blue), while the attentional modulations are shown in red. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
Therefore it is theoretically possible that strong left hemispheric activation in the parietal lobe is present in any counting task regardless of side of stimulation, thereby obscuring a possible activation in the left S1. A fundamental question concerns the functional role of attention in the processing of touch. The fact that in some cases stimuli are as effectively processed regardless whether they are attended or not [14– 16] while in other cases stimulus processing can be facilitated [12], or suppressed [35] leaves one question open. What might attention to tactile events be good for? Unlike lower animal species, in humans the importance of somato-sensory information and the need to filter out relevant from irrelevant tactile events are rather small. With regard to the relevant anatomy, an evolutionary break can be observed between marmosets and macaques, the later possessing much less abundant direct projections from the ventromedial thalamus to S2 than to S1 [36]. For humans much of the perceptual analysis of touch seems to take place without attention [17,18]. This rather small influence of attention on tactile processing is in line with the present finding that the strongest attention-related activation was neither located in the primary (S1) nor in the secondary (S2) somato-sensory cortex. Additional activity was also observed in the supplementary motor area (SMA). These areas are well known to be involved in motor preparation and execution. More importantly, the bilateral activation indicates that the motor preparation is not specific to the attended side, suggesting that attention to somato-sensory events rather leads to a general increase of the activation level of the motor system. This increase in motor activation is compatible with the idea of preparation for the consequence of a subsequent “fight or flight” decision. Previous work interpreted activity in motor-related regions during attention to tactile events in the context of verbal or motor responses that were required in the experiment [27]. Our experiment did not require an explicit motor response, although it could be argued that even without speaking counting per se might trigger implicit motor responses. However, counting was not varied across conditions, i.e. subjects had to count in the attended as well as in the unattended conditions. We therefore think it unlikely that counting elicited the observed activity in bilateral M1 and in the SMA. Our results rather point out to the tight relationship between the somato-sensory and motor system. In an animal decision task experiment Salinas and Romo [37] could observe that cells in the primary motor cortex (M1) in monkeys had different firing patterns depending on the quality of the tactile stimulus. They also could prove that these activated M1 cells were not motor but sensory dependent, because in a control visual reaction task they stopped firing in absence of the tactile stimuli. In primates touch to a body surface triggers an alerting response with subsequent orientation of the eyes and head toward the stimulated site in order to facilitate an appropriate response [38]. This is commensurate with the activation pattern observed in the present
study, and would argue in favor of a similar mechanism in humans. Taken together, the present results lead to the conclusion that in the human species attention in the somato-sensory system might be directly linked to preparatory processing in the motor system. Acknowledgements The authors thank Robert Fendrich for comments on an earlier version of the manuscript. The work was supported by grants Scho 1217/1-1 from the Deutsche Forschungsgemeinschaft (DFG) and 01GO0504 from the Bundesministerium für Bildung und Forschung (BMBF). References [1] Rotte M, Kanowski M, Heinze HJ. Functional magnetic resonance imaging for the evaluation of the motor system: primary and secondary brain areas in different motor tasks. Stereotact Funct Neurosurg 2002;78:3–16. [2] Hillyard SA, Mangun GR. Sensory gating as a physiological mechanism for visual selective attention. Electroencephalogr Clin Neurophysiol Suppl 1987;40:61–7. [3] Schoenfeld MA, Hopf JM, Martinez A, et al. Spatio-temporal analysis of featurebased attention. Cereb Cortex 2007;17:2468–77. [4] Woldorff MG, Liotti M, Seabolt M, Busse L, Lancaster JL, Fox PT. The temporal dynamics of the effects in occipital cortex of visual–spatial selective attention. Brain Res Cogn Brain Res 2002;15:1–15. [5] Schoenfeld MA, Woldorff M, Duzel E, Scheich H, Heinze HJ, Mangun GR. Formfrom-motion: MEG evidence for time course and processing sequence. J Cogn Neurosci 2003;15:157–72. [6] Valdes-Sosa M, Bobes MA, Rodriguez V, Pinilla T. Switching attention without shifting the spotlight object-based attentional modulation of brain potentials. J Cogn Neurosci 1998;10:137–51. [7] Hopf JM, Boehler CN, Luck SJ, Tsotsos JK, Heinze HJ, Schoenfeld MA. Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision. Proc Natl Acad Sci U S A 2006;103:1053–8. [8] Stoppel CM, Boehler CN, Sabelhaus C, Heinze HJ, Hopf JM, Schoenfeld MA. Neural mechanisms of spatial- and feature-based attention: a quantitative analysis. Brain Res 2007;1181:51–60. [9] Noesselt T, Shah NJ, Jancke L. Top-down and bottom-up modulation of language related areas—an fMRI study. BMC Neurosci 2003;4:13. [10] Martinez A, Anllo-Vento L, Sereno MI, et al. Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 1999;2:364–9. [11] Martinez A, DiRusso F, Anllo-Vento L, Sereno MI, Buxton RB, Hillyard SA. Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res 2001;41:1437–57. [12] Evans PM, Craig JC. Response competition: a major source of interference in a tactile identification task. Percept Psychophys 1992;51:199–206. [13] Lloyd DM, Bolanowski Jr SJ, Howard L, McGlone F. Mechanisms of attention in touch. Somatosens Motor Res 1999;16:3–10. [14] Whang KC, Burton H, Shulman GL. Selective attention in vibrotactile tasks: detecting the presence and absence of amplitude change. Percept Psychophys 1991;50: 157–65. [15] Sathian K, Burton H. The role of spatially selective attention in the tactile perception of texture. Percept Psychophys 1991;50:237–48. [16] Bruyant P, Garcia-Larrea L, Mauguiere F. Target side and scalp topography of the somato-sensory P300. Electroencephalogr Clin Neurophysiol 1993;88:468–77. [17] Johansen-Berg H, Lloyd DM. The physiology and psychology of selective attention to touch. Front Biosci 2000;5:D894–904.
98
I. Galazky et al. / Journal of the Neurological Sciences 279 (2009) 93–98
[18] Johansen-Berg H, Christensen V, Woolrich M, Matthews PM. Attention to touch modulates activity in both primary and secondary somato-sensory areas. NeuroReport 2000;11:1237–41. [19] Backes WH, Mess WH, van Kranen-Mastenbroek V, Reulen JP. Somato-sensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention. Clin Neurophysiol 2000;111:1738–44. [20] Arthurs OJ, Johansen-Berg H, Matthews PM, Boniface SJ. Attention differentially modulates the coupling of fMRI BOLD and evoked potential signal amplitudes in the human somato-sensory cortex. Exp Brain Res 2004;157:269–74. [21] Desmedt JE, Tomberg C. Mapping early somato-sensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference the cognitive P30, P40, P100 and N140. Electroencephalogr Clin Neurophysiol 1989;74:321–46. [22] Garcia-Larrea L, Bastuji H, Mauguiere F. Mapping study of somato-sensory evoked potentials during selective spatial attention. Electroencephalogr Clin Neurophysiol 1991;80:201–14. [23] Taylor-Clarke M, Kennett S, Haggard P. Vision modulates somato-sensory cortical processing. Curr Biol 2002;12:233–6. [24] Mima T, Nagamine T, Nakamura K, Shibasaki H. Attention modulates both primary and second somato-sensory cortical activities in humans: a magnetoencephalographic study. J Neurophysiol 1998;80:2215–21. [25] Mauguiere F, Merlet I, Forss N, et al. Activation of a distributed somato-sensory cortical network in the human brain: a dipole modelling study of magnetic fields evoked by median nerve stimulation. Part II: effects of stimulus rate, attention and stimulus detection. Electroencephalogr Clin Neurophysiol 1997;104:290–5. [26] Drevets WC, Burton H, Videen TO, Snyder AZ, Simpson Jr JR, Raichle ME. Blood flow changes in human somato-sensory cortex during anticipated stimulation. Nature 1995;373:249–52. [27] Burton H, Abend NS, MacLeod AM, Sinclair RJ, Snyder AZ, Raichle ME. Tactile attention tasks enhance activation in somato-sensory regions of parietal cortex: a positron emission tomography study. Cereb Cortex 1999;9:662–74.
[28] Meyer E, Ferguson SS, Zatorre RJ, et al. Attention modulates somato-sensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography. Ann Neurol 1991;29:440–3. [29] Staines WR, Graham SJ, Black SE, McIlroy WE. Task-relevant modulation of contralateral and ipsilateral primary somato-sensory cortex and the role of a prefrontal–cortical sensory gating system. NeuroImage 2002;15:190–9. [30] Macaluso E, Frith C, Driver J. Selective spatial attention in vision and touch: unimodal and multimodal mechanisms revealed by PET. J Neurophysiol 2000;83:3062–75. [31] Hamalainen H, Hiltunen J, Titievskaja I. fMRI activations of SI and SII cortices during tactile stimulation depend on attention. Neuroreport 2000;11:1673–6. [32] Hsiao SS, Lane J, Fitzgerald P. Representation of orientation in the somato-sensory system. Behav Brain Res 2002;135:93–103. [33] Hyvarinen J, Poranen A, Jokinen Y. Influence of attentive behavior on neuronal responses to vibration in primary somato-sensory cortex of the monkey. J Neurophysiol 1980;43:870–82. [34] Hamalainen H, Hiltunen J, Titievskaja I. Activation of somato-sensory cortical areas varies with attentional state: an fMRI study. Behav Brain Res 2002;135:159–65. [35] Spence C, Pavani F, Driver J. Crossmodal links between vision and touch in covert endogenous spatial attention. J Exp Psychol Hum Percept Perform 2000;26:1298–319. [36] Zhang HQ, Murray GM, Turman AB, Mackie PD, Coleman GT, Rowe MJ. Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII. J Neurophysiol 1996;76:3633–55. [37] Romo R, Salinas E. Sensing and deciding in the somato-sensory system. Curr Opin Neurobiol 1999;9:487–93. [38] Groh JM, Sparks DL. Saccades to somato-sensory targets. I. Behavioral characteristics. J Neurophysiol 1996;75:412–27. [39] Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somato-sensory cortex. Science 1997;277:968–71.
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Attention to somatosensory events is directly linked to the preparation for action Imke Galazky a,⁎, Hartmut Schütze a,b, Toemme Noesselt a, Jens-Max Hopf a,c, Hans-Jochen Heinze a,c, Mircea Ariel Schoenfeld a,c,d a
Department of Neurology, Otto-von-Guericke University Magdeburg, Germany Department of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, Germany Leibniz Institute for Neurobiology Magdeburg, Germany d Kliniken Schmieder, Allensbach, Germany b c
a r t i c l e
i n f o
Article history: Received 29 April 2008 Received in revised form 1 December 2008 Accepted 3 December 2008 Available online 23 January 2009 Keywords: Somatosensory system Attention to touch fMRI Preparation for action
a b s t r a c t The present study investigated the neural basis of attention in the somato-sensory system. Subjects directed their attention towards their left or right hand while functional MRI data was collected during tactile stimulation of the fingers. Activations evoked by tactile stimuli when a stimulated hand was attended vs. unattended were contrasted. The tactile stimuli elicited hemodynamic responses in the contralateral primary and secondary somatosensory cortex. No attentional modulations of the BOLD-response could be observed in these regions. However, attention-related modulations were observed at more anterior locations in the ipsiand contralateral primary motor cortex and in the supplementary motor area. This pattern of results suggests, that attention to somato-sensory events is directly linked to the motor system and the preparation for action. This mechanism appears to be in stark contrast to visual or auditory attention, which primarily serve to separate relevant from irrelevant information. © 2008 Elsevier B.V. All rights reserved.
1. Introduction From the early days of neuroimaging the somato-sensory system has been subject to extensive research. While the pioneering work mainly employed electrophysiological measures of brain activity now, recently developed methods like functional magnetic resonance imaging (fMRI) offer the possibility of investigating this system in humans with a high spatial resolution. Investigations of the topographical distribution of the activated brain regions can complement the large body of available electrophysiological data and lead towards a deeper understanding of physiological processes. It should be noted that, so far, both hemodynamic and electrophysiological approaches have provided converging evidence on the somatotopic functional organization of the somatosensory cortex, confirming the long-standing knowledge on the “homunculus” in the primary somato-sensory cortex [1]. One of the key questions in the research on sensory systems concerns the role of attention. In the visual and the auditory system attention has been shown to play an eminent role by ‘filtering out’ unwanted information and by enhancing relevant information. These mechanisms enable our brain to deal with the massive input constantly bombarding those sensory systems. Several mechanisms for accomplishing this have been described, some working by enhancing the gain of the wanted information [2–4], other by
⁎ Corresponding author. E-mail address: [email protected] (I. Galazky). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.12.006
suppressing unwanted information [5,6]. Both of these mechanisms might also operate at the same time [7]. It is important to note that these attentional mechanisms operate in those regions in which the sensory processing of the perceived features takes place [8]. A key question, however, concerns the exact level of processing at which the attentional modulations occur. Lately, in the visual system, a growing body of evidence has emerged indicating that the primary visual cortex (area V1) is indeed subject to attentional modulations (reviewed in [9]). While it is currently under discussion whether these modulations in V1 occur during or after the initial flow of activity, there is now no doubt about the fact that activity in area V1 is modulated by attention [10,11]. The picture is less clear for the primary somato-sensory cortex. Animal studies have shown that attention can facilitate [12] but also suppress [13] stimulus processing in this region. Other studies have reported that tactile stimuli are effectively processed regardless whether they are attended or not [14–16]. Nevertheless, there is some evidence that primary and secondary somato-sensory areas might be subject to attentional modulation in humans. Data bearing on this have been provided by somato-sensory evoked potentials (SEP), magnetoencephalography (MEG), positron emission tomography (PET), and fMRI studies [17–29]. While some studies have reported attentional modulations in the primary somato-sensory cortex (S1) using different methodologies [23,26,30], other studies have mainly found activation changes in the secondary somatosensory cortex (S2) [19,29]. Other studies have shown increased activations in both S1 and S2 [27,31] or no difference in the attentional
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modulation between S1 and S2 at all [18]. In general, most of the previous fMRI studies have either found attentional modulations in areas S1 or S2 to be quite small or not present at all [17]. A key question is what aspects of the different studies might have led to the different and in part conflicting results. A close look at the employed experimental designs suggests two important considerations that are germane to this issue. Whenever activity has been found in the primary somato-sensory cortex, it has been rather small in magnitude. Secondly, the likelihood of detecting attentional modulation in this region appears to strongly depend on the choice of the control task. The studies that found such modulations in the primary sensory cortex employed designs in which tactile stimuli had to be actively suppressed in the unattended (control) condition (reviewed in [17]). This observation suggests that the observed modulations in the primary somato-sensory cortex in the attention vs. control contrasts stem from suppression in the unattended control condition rather than from enhanced processing in the attend condition. In order to investigate whether this is indeed the case, we chose a paradigm in which attention is directed towards and away from identical physical stimuli, thereby attempting to avoid sensory confounds. We chose to use a block design because the results would typically be very robust. While tactile stimuli were delivered to fingers II and V of both hands, attention was directed towards or away from one hand, by asking the subjects to either count the stimuli delivered to that hand or those delivered to the other hand. In this way it was possible to compare the activity elicited by exactly the same tactile event (e.g. stimuli delivered to the left index finger) while the left hand was attended (the attended condition for left hand) and while the right hand was attended (the unattended condition for left hand). Since the subject is counting in both cases and the physical stimuli are identical, putative differences in fMRI activity can only be related to the different attention conditions. In contrast to other sensory systems the importance of attention to touch appears to be rather small in humans. Evolutionary and cultural factors like the wearing of clothes have rather made it necessary to suppress input from skin sensors, than enhance their processing. In contrast to many animals, where somato-sensory events are an important alarming signal, there is no essential need to sort out relevant from irrelevant tactile events in humans. This is in line with the findings of most previous studies, in which attentional modulations in the primary somato-sensory cortex were rather small and in most cases only present when stimuli had to be either ignored or actively suppressed in the control task [17]. Consequently, we speculated that in the present study attentional modulations would be rather small in the primary somatosensory cortex and more pronounced in brain regions related to alertness and motor planning. 2. Methods 2.1. Subjects The ethics committee of the University of Magdeburg approved the study. After giving informed consent, fifteen young healthy subjects participated as paid volunteers in this study: nine were women and six were men, mean age 24 years (SD 3, 8, range 22–37). All subjects were right handed.
scanning the pneumatic devices at the fingertips were adjusted until the subject reported equal stimulation intensity at all four stimulation sites. The timing was controlled by a microcomputer and the experiment consisted of four experimental runs of 8 min each. Consequently, each finger (stimulation site) received three blocks of stimulation during an 8 min run. The sequential order of the stimulation sites (blocks) was pseudo-randomized. Before the run started the subjects were verbally instructed to pay attention to one hand (left or right) and to count in mind the stimuli delivered to the fingers of that hand. Stimuli delivered to the other hand were to be ignored during that run. The left and right hand attention conditions were counterbalanced across the four runs. After each run the subjects reported the count of delivered stimuli for each finger of the attended hand. 2.3. MRI data acquisition 2.3.1. fMRI The subjects were scanned in a 1.5 Tesla scanner (General Electric Signa Horizon LX, neuro-optimized, General Electric Inc., Milwaukee, WI, USA) with a standard GE headcoil. The functional images were acquired using a gradient echo single shot echo-planar-imaging (EPI) sequence with time of echo (TE)/time of repetition (TR)/bandwidth/ flip angle = 40 ms/2 s/83 kHz/80°. Twenty-three slices (5 mm thickness, 1 mm gap, field of view 200 mm, matrix 64 × 64) parallel to the anterior–posterior commissure line, covering the full brain were acquired. In each functional run 240 volumes were collected resulting in a scan time of 8 min per run. 2.3.2. Anatomical images Structural MRI was performed in a separate session. A T1-wheigted high resolution data set was acquired using a three dimensional single pulse gradient recovery sequence with TE/TR/flip angle = 8 ms/24 ms/ 30°. In each functional session a T1-weighted EPI (Inversion recovery prepared EPI, TE/TR/time of inversion = 16 ms/12 s/1050 ms) image set was collected with slice parameters identical to the functional data. 2.4. MRI data analysis The MRI data were analyzed using SPM2 (Wellcome Department of Cognitive Neurology). The recorded data were analyzed with the preprocessing routines provided by the package, including realignment, co-registration and spatial normalization to the MNI template. The statistical analyses were carried out on smoothed (8 mm fullwidth Gaussian kernel) images. Two types of comparisons were performed. In order to assess the effect of tactile stimulation, blocks with tactile stimulation delivered to the unattended hand were contrasted with the rest periods for each of the four sites. The effect of attention was revealed contrasting stimulation periods at exactly the same stimulation site (for example the right index finger), when the hand was attended (i.e. subjects counted the number of stimuli delivered to the right hand) vs. unattended (i.e. subjects counted the number of delivered stimuli to the left hand). It is important to note that in these types of comparisons the physical stimulus is always identical (e.g. 20 s tactile stimulation with a pace of 1 Hz delivered to the same fingertip), while attention is manipulated towards and away from the respective hand. A random effects model was employed to perform the group analysis.
2.2. Experimental paradigm 3. Results Subjects were presented with a classical fMRI block design paradigm, consisting of alternating stimulation and pause periods with duration of 20 s each (see Fig. 1). During stimulation blocks tactile stimuli were applied to either the index finger [D2] or to the fifth finger [D5] of the left or the right hand, with a frequency of 1 Hz. The stimuli were delivered using a custom made pneumatic device via plastic tubes carrying compressed air to synthetic membranes taped to the fingertips. Before
3.1. Behavioral results Overall, the subjects made few errors in counting and reporting the correct number of tactile stimuli, with a 96.2% accuracy rate. No significant differences in accuracy were observed between left (97%) and right (95.4%) hand counts F(1,14) = 1.46; p N 0.05.
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Fig. 1. The figure shows a typical experimental run. Subjects were presented with alternating periods of stimulation and rest with duration of 20 s each. Tactile stimuli were applied block-wise to the right index finger [d2r], the right fifth finger [d5r], the left index finger [d2l], and the left fifth finger [d5l] with a frequency of 1 Hz. The experiment was carried out in four experimental runs with a duration of 8 min each. Prior to each run the subjects were instructed to count in mind the stimuli delivered to either the fingers of the right or the left hand. After each run the subjects reported the count of delivered stimuli for each finger of the attended hand.
3.2. Sensory responses to tactile stimulation The activity elicited by tactile stimulation was assessed by comparing blocks of tactile stimulation in unattended conditions vs. the rest periods with no tactile stimulation separately for the left and right hand. Stimulation led to activations of the primary (S1) and secondary (S2) somato-sensory cortex in the contra-lateral hemisphere and in the cingulate gyrus (see Fig. 2). In detail, tactile stimulation of the right fingers elicited activations of the left postcentral gyrus (MNI-coordinates −48/−28/60), the left transverse temporal gyrus (MNI −40/−20/20) and the cingulate gyrus (MNI 0/0/ 40). During tactile stimulation of the left fingers we found activations of the right postcentral gyrus (MNI 44/−24/60), the right lateral sulcus (MNI 40/−20/16) and the cingulate gyrus (MNI 0/−4/40). In both hemispheres clusters of activation during tactile stimulation of the fifth fingers (right D5: MNI −52/−28/48, left D5: MNI 40/−35/54) were localized laterally and posterior to those hemodynamic responses evoked by identical stimulation of the index fingers (right D2: MNI −52/−24/56, left D2: MNI 42/−24/60) (see Fig. 3). 3.3. Attentional modulations In the attention condition tactile stimulation also elicited hemodynamic activity in the contralateral primary somato-sensory cortex (S1), the contralateral secondary somato-sensory cortex (S2) and the cingulate cortex. In addition activation was observed in the supplementary motor area (SMA). Compared to the locations of the activations during tactile stimulation in the absence of attention the attention-related activations were found to be located more laterally and anterior. To investigate which areas are modulated by attention the responses to the identical tactile stimuli in the attended conditions were contrasted with those in unattended conditions. These contrasts revealed activations located in the precentral gyrus in both the
contralateral and ipsilateral hemisphere as well as in the SMA (Fig. 4), but not in the postcentral somatosensory areas. Attention to tactile stimulation of the right fingers elicited hemodynamic responses in the left (MNI −56/−4/44) as well as in the right precentral gyrus (MNI 56/ −4/40) and in the medial frontal gyrus (MNI −4/−8/60). Attention to left hand stimuli led to activations in the right (MNI 56/−4/48) and left precentral gyrus (MNI −52/−8/44) and in the medial frontal gyrus (MNI −4/−4/68). Table 1 shows the reported activations for those conditions. 4. General summary The somato-sensory stimulation elicited activity in the contralateral S1, with a topographical distribution corresponding to the well known homunculus [1]. Additional activity was observed in an area within the cingulate gyrus, which has previously been described to reflect subjective aspects of the stimulation [39]. Importantly, the locations of the attentional modulations did not match the locations of the regions activated in the primary somato-sensory cortex (S1) during tactile stimulation. The revealed attention-related clusters of activation were localized more laterally and anterior (see Fig. 3). Visual inspection and Talairach co-ordinates identified these regions as the primary motor cortex (M1) in the ipsilateral and contralateral hemisphere. In addition to the bilateral primary motor cortex activations, attention related modulations were also observed in the supplementary motor area (SMA). 5. Discussion In the present study, we investigated the neural correlates of attention to tactile stimuli delivered to the index (D2) and little finger (D5) of the left and right hand under attended and unattended conditions. Unattended tactile stimuli elicited hemodynamic activity in the contralateral primary (S1) and secondary somato-sensory
Fig. 2. Group analysis: The figure shows the regions activated during tactile stimulation (red colour: activations during left side stimulation; blue colour: activations during right side stimulation, both contrasted vs. the rest condition) (see also Table 1) across the subjects. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
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Fig. 3. Group analysis: The figure shows the spatial distribution of activations by tactile stimulation of the index finger (red colour) and fifth finger (blue colour) for both hemispheres across the subjects. Note the somatotopic topographical distribution. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
cortex (S2), as well as in the cingulate gyrus (see Fig. 2). The activations in S1 in response to contralateral stimulation delivered to D2 and D5 had slightly different locations, corresponding to the somatotopic organization of this region (the response to D5 stimulation was more lateral and posterior compared to D2 stimulation, see Fig. 3). The location of the activations are fully consistent with findings from electrophysiological recordings (SEP [21–23] and MEG [24,25]). Importantly, when attention was directed to the corresponding hand where the stimuli were delivered, no significant modulations could be observed in S1. An enhancement of activity was observed in regions located more anterior, namely in the primary motor cortex (M1) and in the supplementary motor area (SMA) (see Fig. 4). The modulations in area M1 were observed in both, the ipsilateral and the contralateral hemisphere to the delivered tactile stimulus. These results show that attention to tactile stimuli primarily modulates hemodynamic activity in motor areas, suggesting that this type of attention might be directly involved in the preparation for motor action. Previous studies investigated changes of neuronal activity in the somatosensory cortex under conditions when tactile stimuli were attended vs. unattended. Modulations of activity have been reported using a variety of methods like single unit recordings in monkeys [32,33], SEPs [21–23], MEG [24,25], PET [26–28] and fMRI [17–20,29] in humans. Nevertheless, important questions remained with respect to both the nature of the modulations and their functional role. While enhancement of activity in the primary somato-sensory cortex (S1) has been reported in some fMRI studies [23,30], others have showed decreased activity in areas other than S1 [26], or no modulation at all [18] when using conventional group analysis approaches. A similar puzzle emerges from the findings with regard to the secondary somatosensory cortex (S2). Backes et al. [19] and Staines et al. [29] showed an increased BOLD response in the secondary somato-sensory cortex for
attended vs. unattended somato-sensory stimulation. Other authors reported a simultaneous increase of activations in S1 and S2 [27] or a greater increase in S2 than S1 [34]. However, there are also reports of no difference at all in the attentional modulation between S1 and S2 [18]. In the present study attentional modulation was neither found in the primary (S1) nor in the secondary (S2) somato-sensory cortex. This somewhat surprising result is probably due to the fact that we used a conservative group analysis approach. The small physical size of the effects in these regions paired with inter-individual variability apparently make it difficult to detect changes due to attention at group level [17]. This result replicates the findings of Johansen-Berg et al. [18], who also did not find attentional modulations in S1 or S2 at group level. Nevertheless, this does not mean that S1 or S2 are not modulated at all by attention. Johansen-Berg et al. [18] for example performed a region of interest analysis on their data and were able to find small attentional modulations that were not revealed by the previously performed group analysis. In addition, most of the previous studies reporting attentional modulations in S1 and S2 employed paradigms in which attention was actively withdrawn by distraction in the unattended condition to maximize the effect [20,28] (reviewed in [17]). This is very different from the paradigm used here. It should be kept in mind that the task difficulty in the present experiment was rather low, as indicated by the high accuracy rates in the behavioral data. Consequently, under low attentional load S1 and S2 do not appear to be strongly modulated by attention. S1 and S2 might well be modulated by attention when the task difficulty is increased, or when the allocation of resources is higher due to high attentional load. In addition, the well-known right hemispheric dominance for attentional processing could have contributed to the lack of attentional modulation in S1 found here. Another potential confound arises from the left hemispheric specialization for counting. Often numbers are verbalized or fingers are imagined during counting.
Table 1 Activations for attended and non-attended condition during tactile stimulation of the right and left fingers Condition Non-attended stimulation of the right fingers
Non-attended stimulation of the left fingers
Attended stimulation of the right fingers
Attended stimulation of the left fingers
Anatomical regions Postcentral gyrus Transversal temporal gyrus Cingulate gyrus Postcentral gyrus Lateral cerebral sulcus Cingulate gyrus Contralateral precentral gyrus Ipsilateral precentral gyrus Supplementary motor area Contralateral Precentral gyrus Ipsilateral precentral gyrus Supplementary motor area
Functional description
x
MNI coordinates y
z
S1 S2 – S1 S2 – M1 M1 SMA M1 M1 SMA
−48 −40 0 44 40 0 −56 56 −4 56 −52 −4
−28 −20 0 −24 −20 −4 −4 −4 −8 −4 −8 −8
60 20 40 60 16 40 44 40 60 48 44 68
k
pcorr
18 10 2 61 30 84 72 13 93 5 10 18
0.042 0.001 0.001 0.0001 0.006 0.0001 0.010 0.010 0.013 0.010 0.010 0.053
S1—Primary somatosensory cortex, S2—Secondary somatosensory cortex, SMA—Supplementary motor area, k—number of activated voxels, pcorr—corrected probability for multiple comparisons.
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Fig. 4. Group analysis. The figure shows the spatial distribution of activation patterns elicited by contralateral (unattended) tactile stimulation (in blue), while the attentional modulations are shown in red. The activations are thresholded at p b 0.01 corrected for multiple comparisons with a cluster criterion of 5 voxels.
Therefore it is theoretically possible that strong left hemispheric activation in the parietal lobe is present in any counting task regardless of side of stimulation, thereby obscuring a possible activation in the left S1. A fundamental question concerns the functional role of attention in the processing of touch. The fact that in some cases stimuli are as effectively processed regardless whether they are attended or not [14– 16] while in other cases stimulus processing can be facilitated [12], or suppressed [35] leaves one question open. What might attention to tactile events be good for? Unlike lower animal species, in humans the importance of somato-sensory information and the need to filter out relevant from irrelevant tactile events are rather small. With regard to the relevant anatomy, an evolutionary break can be observed between marmosets and macaques, the later possessing much less abundant direct projections from the ventromedial thalamus to S2 than to S1 [36]. For humans much of the perceptual analysis of touch seems to take place without attention [17,18]. This rather small influence of attention on tactile processing is in line with the present finding that the strongest attention-related activation was neither located in the primary (S1) nor in the secondary (S2) somato-sensory cortex. Additional activity was also observed in the supplementary motor area (SMA). These areas are well known to be involved in motor preparation and execution. More importantly, the bilateral activation indicates that the motor preparation is not specific to the attended side, suggesting that attention to somato-sensory events rather leads to a general increase of the activation level of the motor system. This increase in motor activation is compatible with the idea of preparation for the consequence of a subsequent “fight or flight” decision. Previous work interpreted activity in motor-related regions during attention to tactile events in the context of verbal or motor responses that were required in the experiment [27]. Our experiment did not require an explicit motor response, although it could be argued that even without speaking counting per se might trigger implicit motor responses. However, counting was not varied across conditions, i.e. subjects had to count in the attended as well as in the unattended conditions. We therefore think it unlikely that counting elicited the observed activity in bilateral M1 and in the SMA. Our results rather point out to the tight relationship between the somato-sensory and motor system. In an animal decision task experiment Salinas and Romo [37] could observe that cells in the primary motor cortex (M1) in monkeys had different firing patterns depending on the quality of the tactile stimulus. They also could prove that these activated M1 cells were not motor but sensory dependent, because in a control visual reaction task they stopped firing in absence of the tactile stimuli. In primates touch to a body surface triggers an alerting response with subsequent orientation of the eyes and head toward the stimulated site in order to facilitate an appropriate response [38]. This is commensurate with the activation pattern observed in the present
study, and would argue in favor of a similar mechanism in humans. Taken together, the present results lead to the conclusion that in the human species attention in the somato-sensory system might be directly linked to preparatory processing in the motor system. Acknowledgements The authors thank Robert Fendrich for comments on an earlier version of the manuscript. The work was supported by grants Scho 1217/1-1 from the Deutsche Forschungsgemeinschaft (DFG) and 01GO0504 from the Bundesministerium für Bildung und Forschung (BMBF). References [1] Rotte M, Kanowski M, Heinze HJ. Functional magnetic resonance imaging for the evaluation of the motor system: primary and secondary brain areas in different motor tasks. Stereotact Funct Neurosurg 2002;78:3–16. [2] Hillyard SA, Mangun GR. Sensory gating as a physiological mechanism for visual selective attention. Electroencephalogr Clin Neurophysiol Suppl 1987;40:61–7. [3] Schoenfeld MA, Hopf JM, Martinez A, et al. Spatio-temporal analysis of featurebased attention. Cereb Cortex 2007;17:2468–77. [4] Woldorff MG, Liotti M, Seabolt M, Busse L, Lancaster JL, Fox PT. The temporal dynamics of the effects in occipital cortex of visual–spatial selective attention. Brain Res Cogn Brain Res 2002;15:1–15. [5] Schoenfeld MA, Woldorff M, Duzel E, Scheich H, Heinze HJ, Mangun GR. Formfrom-motion: MEG evidence for time course and processing sequence. J Cogn Neurosci 2003;15:157–72. [6] Valdes-Sosa M, Bobes MA, Rodriguez V, Pinilla T. Switching attention without shifting the spotlight object-based attentional modulation of brain potentials. J Cogn Neurosci 1998;10:137–51. [7] Hopf JM, Boehler CN, Luck SJ, Tsotsos JK, Heinze HJ, Schoenfeld MA. Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision. Proc Natl Acad Sci U S A 2006;103:1053–8. [8] Stoppel CM, Boehler CN, Sabelhaus C, Heinze HJ, Hopf JM, Schoenfeld MA. Neural mechanisms of spatial- and feature-based attention: a quantitative analysis. Brain Res 2007;1181:51–60. [9] Noesselt T, Shah NJ, Jancke L. Top-down and bottom-up modulation of language related areas—an fMRI study. BMC Neurosci 2003;4:13. [10] Martinez A, Anllo-Vento L, Sereno MI, et al. Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 1999;2:364–9. [11] Martinez A, DiRusso F, Anllo-Vento L, Sereno MI, Buxton RB, Hillyard SA. Putting spatial attention on the map: timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res 2001;41:1437–57. [12] Evans PM, Craig JC. Response competition: a major source of interference in a tactile identification task. Percept Psychophys 1992;51:199–206. [13] Lloyd DM, Bolanowski Jr SJ, Howard L, McGlone F. Mechanisms of attention in touch. Somatosens Motor Res 1999;16:3–10. [14] Whang KC, Burton H, Shulman GL. Selective attention in vibrotactile tasks: detecting the presence and absence of amplitude change. Percept Psychophys 1991;50: 157–65. [15] Sathian K, Burton H. The role of spatially selective attention in the tactile perception of texture. Percept Psychophys 1991;50:237–48. [16] Bruyant P, Garcia-Larrea L, Mauguiere F. Target side and scalp topography of the somato-sensory P300. Electroencephalogr Clin Neurophysiol 1993;88:468–77. [17] Johansen-Berg H, Lloyd DM. The physiology and psychology of selective attention to touch. Front Biosci 2000;5:D894–904.
98
I. Galazky et al. / Journal of the Neurological Sciences 279 (2009) 93–98
[18] Johansen-Berg H, Christensen V, Woolrich M, Matthews PM. Attention to touch modulates activity in both primary and secondary somato-sensory areas. NeuroReport 2000;11:1237–41. [19] Backes WH, Mess WH, van Kranen-Mastenbroek V, Reulen JP. Somato-sensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention. Clin Neurophysiol 2000;111:1738–44. [20] Arthurs OJ, Johansen-Berg H, Matthews PM, Boniface SJ. Attention differentially modulates the coupling of fMRI BOLD and evoked potential signal amplitudes in the human somato-sensory cortex. Exp Brain Res 2004;157:269–74. [21] Desmedt JE, Tomberg C. Mapping early somato-sensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference the cognitive P30, P40, P100 and N140. Electroencephalogr Clin Neurophysiol 1989;74:321–46. [22] Garcia-Larrea L, Bastuji H, Mauguiere F. Mapping study of somato-sensory evoked potentials during selective spatial attention. Electroencephalogr Clin Neurophysiol 1991;80:201–14. [23] Taylor-Clarke M, Kennett S, Haggard P. Vision modulates somato-sensory cortical processing. Curr Biol 2002;12:233–6. [24] Mima T, Nagamine T, Nakamura K, Shibasaki H. Attention modulates both primary and second somato-sensory cortical activities in humans: a magnetoencephalographic study. J Neurophysiol 1998;80:2215–21. [25] Mauguiere F, Merlet I, Forss N, et al. Activation of a distributed somato-sensory cortical network in the human brain: a dipole modelling study of magnetic fields evoked by median nerve stimulation. Part II: effects of stimulus rate, attention and stimulus detection. Electroencephalogr Clin Neurophysiol 1997;104:290–5. [26] Drevets WC, Burton H, Videen TO, Snyder AZ, Simpson Jr JR, Raichle ME. Blood flow changes in human somato-sensory cortex during anticipated stimulation. Nature 1995;373:249–52. [27] Burton H, Abend NS, MacLeod AM, Sinclair RJ, Snyder AZ, Raichle ME. Tactile attention tasks enhance activation in somato-sensory regions of parietal cortex: a positron emission tomography study. Cereb Cortex 1999;9:662–74.
[28] Meyer E, Ferguson SS, Zatorre RJ, et al. Attention modulates somato-sensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography. Ann Neurol 1991;29:440–3. [29] Staines WR, Graham SJ, Black SE, McIlroy WE. Task-relevant modulation of contralateral and ipsilateral primary somato-sensory cortex and the role of a prefrontal–cortical sensory gating system. NeuroImage 2002;15:190–9. [30] Macaluso E, Frith C, Driver J. Selective spatial attention in vision and touch: unimodal and multimodal mechanisms revealed by PET. J Neurophysiol 2000;83:3062–75. [31] Hamalainen H, Hiltunen J, Titievskaja I. fMRI activations of SI and SII cortices during tactile stimulation depend on attention. Neuroreport 2000;11:1673–6. [32] Hsiao SS, Lane J, Fitzgerald P. Representation of orientation in the somato-sensory system. Behav Brain Res 2002;135:93–103. [33] Hyvarinen J, Poranen A, Jokinen Y. Influence of attentive behavior on neuronal responses to vibration in primary somato-sensory cortex of the monkey. J Neurophysiol 1980;43:870–82. [34] Hamalainen H, Hiltunen J, Titievskaja I. Activation of somato-sensory cortical areas varies with attentional state: an fMRI study. Behav Brain Res 2002;135:159–65. [35] Spence C, Pavani F, Driver J. Crossmodal links between vision and touch in covert endogenous spatial attention. J Exp Psychol Hum Percept Perform 2000;26:1298–319. [36] Zhang HQ, Murray GM, Turman AB, Mackie PD, Coleman GT, Rowe MJ. Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII. J Neurophysiol 1996;76:3633–55. [37] Romo R, Salinas E. Sensing and deciding in the somato-sensory system. Curr Opin Neurobiol 1999;9:487–93. [38] Groh JM, Sparks DL. Saccades to somato-sensory targets. I. Behavioral characteristics. J Neurophysiol 1996;75:412–27. [39] Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somato-sensory cortex. Science 1997;277:968–71.