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Somatosensation: Putting Touch On the Map
Dispatch R119
Somatosensation: Putting Touch On the Map A new study takes a significant step towards uncovering the mechanisms that put tactile events on the brain’s spatial map by establishing a causal link between attention-related parietal alpha oscillatory activity and the external spatial coding of touch. T. Heed Selection of action targets as well as the planning of movements towards them is one of the key roles of posterior parietal cortex. Based on neurophysiological studies of the macaque’s lateral intraparietal area, it has been suggested that posterior parietal cortex selectively represents salient stimuli in saliency or priority maps [1]. These may subserve action selection and, subsequently, movement planning toward the most adequate, currently available stimulus [2]. In humans, the putative homologue of the posterior parietal cortex is located along the medial side of the intraparietal sulcus [3]. In line with the idea of priority mapping, this part of cortex is active during deployment of spatial attention [4]. Spatial attentional processing is accompanied by parietal alpha oscillations, that is, rhythmic firing patterns of entire neuronal populations at about 10 Hz that are measurable with electroencephalography (EEG) and magnetoencephalography (MEG) [5]. Recently, transracial magnetic stimulation (TMS) has been used to apply trains of magnetic pulses over medial intraparietal sulcus to induce alpha oscillatory activity in the stimulated region [6]. Modulation of the ability to detect visual target stimuli suggested a causal role of alpha activity for the deployment of visual attention. A new study by Ruzzoli and Soto-Faraco [7], reported in this issue of Current Biology, extends these findings, demonstrating that alpha entrainment of the same posterior parietal cortex region biases tactile perception in a manner similar to that reported for visual stimuli. Ruzzoli and Soto-Faraco [7] presented participants with a difficult tactile discrimination task. In each trial, participants received one of two slightly different tactile stimuli, presented randomly to the right or left hand. Participants had to identify the
stimulus, independent of which hand was stimulated. Shortly before stimulus presentation, the authors entrained medial intraparietal sulcus, using either an alpha frequency (10 Hz), or one of two alternative frequencies (5 or 20 Hz). They report two key results. First, entraining medial intraparietal sulcus led to asymmetric discrimination performance, with higher performance at the ipsilateral hand; this effect was selective for alpha frequency TMS. Second, when participants crossed their hands, the discrimination bias reversed, with better performance at the contralateral hand — the hand now located in ipsilateral space. Parietal alpha oscillatory activity is inversely related to attentional processing. Thus, higher oscillatory alpha activity in a hemisphere coincides with lower attentional deployment to contralateral space [8,9] (Figure 1A). Accordingly, visual detection was found to be impaired contralateral, but improved ipsilateral to TMS alpha entrainment [6]. In line with these findings, in Ruzzoli and Soto-Faraco’s study [7], alpha entrainment improved performance ipsilaterally, suggesting that TMS caused a relative shift of attention towards the space ipsilateral to alpha TMS. Crucially, the performance modulation evoked by alpha TMS entrainment unfolded in external space, that is, it improved detection at the hand located in the space ipsilateral to alpha induction, rather than at the hand of the anatomically same side as the hemisphere stimulated with TMS. One possible interpretation of these results is that the parietal priority map highlights spatial locations or events independent of stimulus modality. This is far from trivial: recall that TMS affected different hands, depending on hand posture. Thus, tactile stimuli must have been spatially recoded by integrating skin location and hand posture to match touch location with the prioritized, external space. How
does the brain achieve this tactile remapping? Touch first arrives in cortex at the primary somatosensory cortex. This region is known for its homuncular organization, that is, the arrangement of neurons is determined by the arrangement of receptors on the skin. Posture does not appear to modulate neural responses of primary somatosensory cortex. Intraparietal sulcus is known to be involved in many types of coordinate transformations [10,11], making it a prime candidate also for remapping skin-based somatosensory information. In monkeys, an area at the fundus of the intraparietal sulcus, the ventral intraparietal area, appears to align the tactile, auditory, and visual space around the body [11]. In humans, TMS targeted at the putatively homologue region disrupted tactile remapping [12] (Figure 1B, red region). This intraparietal sulcus region is a close neighbor to the one targeted in Ruzzoli and Soto-Faraco’s study (Figure 1B, yellow region). Although it remains to be seen how well TMS can separately target these two neighboring intraparietal sulcus regions, it is tempting to speculate about their functional relationship and the coordinate systems they use. The brain appears to keep both external and skin-based tactile information available during tactile processing [13]. One alternative is that the more lateral region, the putative human homologue of the ventral intraparietal area, provides stimulus information in different coordinates [14]. Other regions might read out spatial information in the reference frame that benefits their current process [15]. The medial intraparietal sulcus region (possibly the human homologue of the lateral intraparietal area) may read out tactile stimulus location in eye-centered coordinates, given that this region codes space in this reference frame for different purposes like attentional deployment [4] and motor planning [16]. However, the medial intraparietal sulcus region may, instead, itself represent different reference frames [17] and take part in the spatial transformation process, given that different subregions of intraparietal sulcus appear to belong to different function-specific frontal-parietal networks [18]. Further experimentation is therefore required
Current Biology Vol 24 No 3 R120
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Figure 1. Illustration of the experimental rationale of Ruzzoli and Soto-Faraco’s TMS study [7]. (A) Alpha oscillatory activity is thought to affect attentional deployment. High alpha activity in a hemisphere reduces attentional deployment to the contralateral space. Here, the disbalance of alpha activity between the two hemispheres biases visual attention to the right (blue region on screen). (B) To test the role of alpha oscillatory activity in touch, rhythmic TMS was applied to a medial intraparietal region (indicated in yellow). The idea is to experimentally create a disbalance of alpha activity between the hemispheres, and thus to selectively affect discrimination performance in one side of space for touch. A previously investigated, more lateral region known to be involved in tactile remapping is indicated in red.
to unravel the specifics underlying the implementation of tactile remapping in posterior parietal cortex, as well as the functional role of alpha oscillatory activity in these regions. There are many more questions that currently remain unanswered. Establishing homology between human and monkey parietal brain areas has been tentative, given significant expansion of parietal cortex and the existence of additional areas in the human brain, as compared to the macaque [19]. Given the spatial proximity of the different regions along the intraparietal sulcus, it is difficult, if not impossible, to separate their oscillatory activity with EEG and MEG in the human brain. The development of TMS techniques that allow manipulating specific neural signatures like neural oscillations therefore raise exciting new possibilities for neuro-cognitive research. Despite limitations in the spatial resolution of TMS, such techniques promise to reach beyond uncovering the architecture of the neural networks underlying parietal function, addressing in addition the functional mechanisms of neural communication within these networks. With their elegant tactile localization study, Ruzzoli and Soto-Faraco [7] demonstrate an important step in this direction. References 1. Gottlieb, J.P., Kusunoki, M., and Goldberg, M.E. (1998). The representation of visual salience in monkey parietal cortex. Nature 391, 481–484.
2. Andersen, R.A., and Cui, H. (2009). Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63, 568–583. 3. Grefkes, C., and Fink, G.R. (2005). The functional organization of the intraparietal sulcus in humans and monkeys. J. Anat. 207, 3–17. 4. Corbetta, M., Akbudak, E., Conturo, T.E., Snyder, A.Z., Ollinger, J.M., Drury, H.A., Linenweber, M.R., Petersen, S.E., Raichle, M.E., Van Essen, D.C., et al. (1998). A common network of functional areas for attention and eye movements. Neuron 21, 761–773. 5. Rihs, T.A., Michel, C.M., and Thut, G. (2007). Mechanisms of selective inhibition in visual spatial attention are indexed by a-band EEG synchronization. Eur. J. Neurosci. 25, 603–610. 6. Romei, V., Gross, J., and Thut, G. (2010). On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J. Neurosci. 30, 8692–8697. 7. Ruzzoli, M., and Soto-Faraco, S. (2014). Alpha stimulation of the human parietal cortex attunes tactile perception to external space. Curr. Biol. 24, 329–332. 8. Sauseng, P., Klimesch, W., Stadler, W., Schabus, M., Doppelmayr, M., Hanslmayr, S., Gruber, W.R., and Birbaumer, N. (2005). A shift of visual spatial attention is selectively
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associated with human EEG alpha activity. Eur. J. Neurosci. 22, 2917–2926. Hanslmayr, S., Aslan, A., Staudigl, T., Klimesch, W., Herrmann, C.S., and Ba¨uml, K.-H. (2007). Prestimulus oscillations predict visual perception performance between and within subjects. NeuroImage 37, 1465–1473. Buneo, C.A., and Andersen, R.A. (2006). The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44, 2594–2606. Graziano, M.S.A., and Cooke, D.F. (2006). Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44, 845–859. Azan˜o´n, E., Longo, M.R., Soto-Faraco, S., and Haggard, P. (2010). The posterior parietal cortex remaps touch into external space. Curr. Biol. 20, 1304–1309. Heed, T., and Ro¨der, B. (2010). Common anatomical and external coding for hands and feet in tactile attention: evidence from event-related potentials. J. Cogn. Neurosci. 22, 184–202. Schlack, A., Sterbing-D’Angelo, S.J., Hartung, K., Hoffmann, K.-P., and Bremmer, F. (2005). Multisensory space representations in the macaque ventral intraparietal area. J. Neurosci. 25, 4616–4625. Pouget, A., Deneve, S., and Duhamel, J.-R. (2002). A computational perspective on the neural basis of multisensory spatial representations. Nat. Rev. Neurosci. 3, 741–747. Medendorp, W.P., Goltz, H.C., Crawford, J.D., and Vilis, T. (2005). Integration of target and effector information in human posterior parietal cortex for the planning of action. J. Neurophysiol. 93, 954–962. Stricanne, B., Andersen, R.A., and Mazzoni, P. (1996). Eye-centered, head-centered, and intermediate coding of remembered sound locations in area lateral intraparietal area. J. Neurophysiol. 76, 2071–2076. Rizzolatti, G., Luppino, G., and Matelli, M. (1998). The organization of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol. 106, 283–296. Krubitzer, L., and Disbrow, E. (2008). The Evolution of Parietal Areas Involved in Hand Use in Primates (Somatosensation Lond.: Elsevier), pp. 183–214.
Biological Psychology and Neuropsychology, Faculty of Psychology and Movement Science, University of Hamburg, 20146 Hamburg, Germany. E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2013.12.037
Evolution: The Making of Ediacaran Giants Some of the enigmatic Precambrian organisms in the Ediacaran Period grew large and stood tall above the seafloor. Canopy flow modeling suggests that their large size was optimized for access to flow in order to facilitate osmotrophic nutrient uptake in low-flow environments. Shuhai Xiao The fuse to the Cambrian explosion — the seemingly sudden appearance of
animal phyla as we know them — is probably buried in the Ediacaran Period (635–541 million years ago, Ma) [1]. The past ten years have seen
Somatosensation: Putting Touch On the Map A new study takes a significant step towards uncovering the mechanisms that put tactile events on the brain’s spatial map by establishing a causal link between attention-related parietal alpha oscillatory activity and the external spatial coding of touch. T. Heed Selection of action targets as well as the planning of movements towards them is one of the key roles of posterior parietal cortex. Based on neurophysiological studies of the macaque’s lateral intraparietal area, it has been suggested that posterior parietal cortex selectively represents salient stimuli in saliency or priority maps [1]. These may subserve action selection and, subsequently, movement planning toward the most adequate, currently available stimulus [2]. In humans, the putative homologue of the posterior parietal cortex is located along the medial side of the intraparietal sulcus [3]. In line with the idea of priority mapping, this part of cortex is active during deployment of spatial attention [4]. Spatial attentional processing is accompanied by parietal alpha oscillations, that is, rhythmic firing patterns of entire neuronal populations at about 10 Hz that are measurable with electroencephalography (EEG) and magnetoencephalography (MEG) [5]. Recently, transracial magnetic stimulation (TMS) has been used to apply trains of magnetic pulses over medial intraparietal sulcus to induce alpha oscillatory activity in the stimulated region [6]. Modulation of the ability to detect visual target stimuli suggested a causal role of alpha activity for the deployment of visual attention. A new study by Ruzzoli and Soto-Faraco [7], reported in this issue of Current Biology, extends these findings, demonstrating that alpha entrainment of the same posterior parietal cortex region biases tactile perception in a manner similar to that reported for visual stimuli. Ruzzoli and Soto-Faraco [7] presented participants with a difficult tactile discrimination task. In each trial, participants received one of two slightly different tactile stimuli, presented randomly to the right or left hand. Participants had to identify the
stimulus, independent of which hand was stimulated. Shortly before stimulus presentation, the authors entrained medial intraparietal sulcus, using either an alpha frequency (10 Hz), or one of two alternative frequencies (5 or 20 Hz). They report two key results. First, entraining medial intraparietal sulcus led to asymmetric discrimination performance, with higher performance at the ipsilateral hand; this effect was selective for alpha frequency TMS. Second, when participants crossed their hands, the discrimination bias reversed, with better performance at the contralateral hand — the hand now located in ipsilateral space. Parietal alpha oscillatory activity is inversely related to attentional processing. Thus, higher oscillatory alpha activity in a hemisphere coincides with lower attentional deployment to contralateral space [8,9] (Figure 1A). Accordingly, visual detection was found to be impaired contralateral, but improved ipsilateral to TMS alpha entrainment [6]. In line with these findings, in Ruzzoli and Soto-Faraco’s study [7], alpha entrainment improved performance ipsilaterally, suggesting that TMS caused a relative shift of attention towards the space ipsilateral to alpha TMS. Crucially, the performance modulation evoked by alpha TMS entrainment unfolded in external space, that is, it improved detection at the hand located in the space ipsilateral to alpha induction, rather than at the hand of the anatomically same side as the hemisphere stimulated with TMS. One possible interpretation of these results is that the parietal priority map highlights spatial locations or events independent of stimulus modality. This is far from trivial: recall that TMS affected different hands, depending on hand posture. Thus, tactile stimuli must have been spatially recoded by integrating skin location and hand posture to match touch location with the prioritized, external space. How
does the brain achieve this tactile remapping? Touch first arrives in cortex at the primary somatosensory cortex. This region is known for its homuncular organization, that is, the arrangement of neurons is determined by the arrangement of receptors on the skin. Posture does not appear to modulate neural responses of primary somatosensory cortex. Intraparietal sulcus is known to be involved in many types of coordinate transformations [10,11], making it a prime candidate also for remapping skin-based somatosensory information. In monkeys, an area at the fundus of the intraparietal sulcus, the ventral intraparietal area, appears to align the tactile, auditory, and visual space around the body [11]. In humans, TMS targeted at the putatively homologue region disrupted tactile remapping [12] (Figure 1B, red region). This intraparietal sulcus region is a close neighbor to the one targeted in Ruzzoli and Soto-Faraco’s study (Figure 1B, yellow region). Although it remains to be seen how well TMS can separately target these two neighboring intraparietal sulcus regions, it is tempting to speculate about their functional relationship and the coordinate systems they use. The brain appears to keep both external and skin-based tactile information available during tactile processing [13]. One alternative is that the more lateral region, the putative human homologue of the ventral intraparietal area, provides stimulus information in different coordinates [14]. Other regions might read out spatial information in the reference frame that benefits their current process [15]. The medial intraparietal sulcus region (possibly the human homologue of the lateral intraparietal area) may read out tactile stimulus location in eye-centered coordinates, given that this region codes space in this reference frame for different purposes like attentional deployment [4] and motor planning [16]. However, the medial intraparietal sulcus region may, instead, itself represent different reference frames [17] and take part in the spatial transformation process, given that different subregions of intraparietal sulcus appear to belong to different function-specific frontal-parietal networks [18]. Further experimentation is therefore required
Current Biology Vol 24 No 3 R120
9.
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Figure 1. Illustration of the experimental rationale of Ruzzoli and Soto-Faraco’s TMS study [7]. (A) Alpha oscillatory activity is thought to affect attentional deployment. High alpha activity in a hemisphere reduces attentional deployment to the contralateral space. Here, the disbalance of alpha activity between the two hemispheres biases visual attention to the right (blue region on screen). (B) To test the role of alpha oscillatory activity in touch, rhythmic TMS was applied to a medial intraparietal region (indicated in yellow). The idea is to experimentally create a disbalance of alpha activity between the hemispheres, and thus to selectively affect discrimination performance in one side of space for touch. A previously investigated, more lateral region known to be involved in tactile remapping is indicated in red.
to unravel the specifics underlying the implementation of tactile remapping in posterior parietal cortex, as well as the functional role of alpha oscillatory activity in these regions. There are many more questions that currently remain unanswered. Establishing homology between human and monkey parietal brain areas has been tentative, given significant expansion of parietal cortex and the existence of additional areas in the human brain, as compared to the macaque [19]. Given the spatial proximity of the different regions along the intraparietal sulcus, it is difficult, if not impossible, to separate their oscillatory activity with EEG and MEG in the human brain. The development of TMS techniques that allow manipulating specific neural signatures like neural oscillations therefore raise exciting new possibilities for neuro-cognitive research. Despite limitations in the spatial resolution of TMS, such techniques promise to reach beyond uncovering the architecture of the neural networks underlying parietal function, addressing in addition the functional mechanisms of neural communication within these networks. With their elegant tactile localization study, Ruzzoli and Soto-Faraco [7] demonstrate an important step in this direction. References 1. Gottlieb, J.P., Kusunoki, M., and Goldberg, M.E. (1998). The representation of visual salience in monkey parietal cortex. Nature 391, 481–484.
2. Andersen, R.A., and Cui, H. (2009). Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63, 568–583. 3. Grefkes, C., and Fink, G.R. (2005). The functional organization of the intraparietal sulcus in humans and monkeys. J. Anat. 207, 3–17. 4. Corbetta, M., Akbudak, E., Conturo, T.E., Snyder, A.Z., Ollinger, J.M., Drury, H.A., Linenweber, M.R., Petersen, S.E., Raichle, M.E., Van Essen, D.C., et al. (1998). A common network of functional areas for attention and eye movements. Neuron 21, 761–773. 5. Rihs, T.A., Michel, C.M., and Thut, G. (2007). Mechanisms of selective inhibition in visual spatial attention are indexed by a-band EEG synchronization. Eur. J. Neurosci. 25, 603–610. 6. Romei, V., Gross, J., and Thut, G. (2010). On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J. Neurosci. 30, 8692–8697. 7. Ruzzoli, M., and Soto-Faraco, S. (2014). Alpha stimulation of the human parietal cortex attunes tactile perception to external space. Curr. Biol. 24, 329–332. 8. Sauseng, P., Klimesch, W., Stadler, W., Schabus, M., Doppelmayr, M., Hanslmayr, S., Gruber, W.R., and Birbaumer, N. (2005). A shift of visual spatial attention is selectively
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associated with human EEG alpha activity. Eur. J. Neurosci. 22, 2917–2926. Hanslmayr, S., Aslan, A., Staudigl, T., Klimesch, W., Herrmann, C.S., and Ba¨uml, K.-H. (2007). Prestimulus oscillations predict visual perception performance between and within subjects. NeuroImage 37, 1465–1473. Buneo, C.A., and Andersen, R.A. (2006). The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44, 2594–2606. Graziano, M.S.A., and Cooke, D.F. (2006). Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44, 845–859. Azan˜o´n, E., Longo, M.R., Soto-Faraco, S., and Haggard, P. (2010). The posterior parietal cortex remaps touch into external space. Curr. Biol. 20, 1304–1309. Heed, T., and Ro¨der, B. (2010). Common anatomical and external coding for hands and feet in tactile attention: evidence from event-related potentials. J. Cogn. Neurosci. 22, 184–202. Schlack, A., Sterbing-D’Angelo, S.J., Hartung, K., Hoffmann, K.-P., and Bremmer, F. (2005). Multisensory space representations in the macaque ventral intraparietal area. J. Neurosci. 25, 4616–4625. Pouget, A., Deneve, S., and Duhamel, J.-R. (2002). A computational perspective on the neural basis of multisensory spatial representations. Nat. Rev. Neurosci. 3, 741–747. Medendorp, W.P., Goltz, H.C., Crawford, J.D., and Vilis, T. (2005). Integration of target and effector information in human posterior parietal cortex for the planning of action. J. Neurophysiol. 93, 954–962. Stricanne, B., Andersen, R.A., and Mazzoni, P. (1996). Eye-centered, head-centered, and intermediate coding of remembered sound locations in area lateral intraparietal area. J. Neurophysiol. 76, 2071–2076. Rizzolatti, G., Luppino, G., and Matelli, M. (1998). The organization of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol. 106, 283–296. Krubitzer, L., and Disbrow, E. (2008). The Evolution of Parietal Areas Involved in Hand Use in Primates (Somatosensation Lond.: Elsevier), pp. 183–214.
Biological Psychology and Neuropsychology, Faculty of Psychology and Movement Science, University of Hamburg, 20146 Hamburg, Germany. E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2013.12.037
Evolution: The Making of Ediacaran Giants Some of the enigmatic Precambrian organisms in the Ediacaran Period grew large and stood tall above the seafloor. Canopy flow modeling suggests that their large size was optimized for access to flow in order to facilitate osmotrophic nutrient uptake in low-flow environments. Shuhai Xiao The fuse to the Cambrian explosion — the seemingly sudden appearance of
animal phyla as we know them — is probably buried in the Ediacaran Period (635–541 million years ago, Ma) [1]. The past ten years have seen