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provided by Elsevier - Publisher Connector Current Biology Vol 16 No 20 R884

of FtsZ are regulated by GTP hydrolysis. a spiral-like intermediate of the bacterial Department of Microbiology and J. Bacteriol. 182, 164–170. cytokinetic protein FtsZ. J. Bacteriol. 188, Molecular Genetics, University of Texas 18. Thanedar, S., and Margolin, W. (2004). 1680–1690. Medical School, 6431 Fannin Street, FtsZ exhibits rapid movement and 20. Quardokus, E., Din, N., and Brun, Y.V. oscillation waves in helix-like patterns (1996). Cell cycle regulation and cell Houston, Texas 77030, USA. in Escherichia coli. Curr. Biol. 14, type-specific localization of the FtsZ E-mail: [email protected] 1167–1173. division initiation protein in Caulobacter. 19. Michie, K.A., Monahan, L.G., Beech, P.L., Proc. Natl. Acad. Sci. USA 93, and Harry, E.J. (2006). Trapping of 6314–6319. DOI: 10.1016/j.cub.2006.09.025

Sensory Neuroscience: From Skin suggesting integration of information from several skin to Object in the Somatosensory locations. Fitzgerald et al. [5] took an approach that had previously Cortex been used to characterise early tactile coding in SI, and applied it to SII neurons, while stimulating the Humans can perceive the shape of objects by touch alone, by extracting animal at several different skin geometric features such as edges. Recently recorded responses of locations. The original method single neurons in the secondary somatosensory cortex of monkeys involved applying an oriented bar suggest how the brain integrates tactile shape information across to the digit pad of a monkey, different regions of skin and builds up a representation of tactile objects. and identifying how the neural response varies with the Patrick Haggard perception of tactile objects is orientation of the bar. In the new unclear. How are multiple study, recordings were made The sense of touch differs from the sensations of contact processed from SII neurons while the pads of other senses because of two and integrated across several each digit on the contralateral hand fundamental features of its different skin locations and at were stimulated, on separate receptor surface, the skin. First, the different times to build up a occasions. Thus, although only one skin is more extensive and more representation of the touched pad was stimulated on any given distributed than other receptor object? trial, the authors could build up surfaces, such as the retina or From computational theories of a picture of each neuron’s the cochlea. Second, the skin visual processing, two critical responses and orientation directly interacts with the stages in computing tactile shape preferences across the different stimulus itself. For example, can be identified: the integration of pads. recognising an object by touch information from different skin often involves actively exploring or locations; and the detection of Receptive Field Shapes manipulating it. Voluntary basic geometric features such as In the second paper, Fitzgerald exploratory actions bring several edges. Two recent papers by et al. [5] report that most of the 928 points on the receptor surface Fitzgerald and colleagues [4,5] neurons studied did respond to the into contact with the object on report evidence for both of these touch of the bar, but their firing rate multiple occasions [1], as when computations within the did not vary with bar orientation. feeling for a particular shape of secondary somatosensory cortex These untuned cells could have coin among many coins in one’s (SII). The first paper [4] deals excitatory (36%) or inhibitory (17%) pocket. with orientation selectivity, while responses to the bar. The response Most neurophysiological studies the second [5] concerns the was measured at each of 12 of touch, however, have passively integration of information from locations, by stimulating the distal, stimulated a single skin location, different skin locations. I will medial and proximal pads of digits using simple stimuli, while begin by discussing the second 2–5 of the contralateral hand. While recording from single units in the paper. many neurons responded to primary somatosensory cortex of SII is a key area for tactile touch on only one finger pad, many monkeys. Thus, areas 3B and 1 of integration: it receives inputs from others responded to touch on the primary somatosensory cortex the adjacent SI region and also several pads, or even on all 12. contain a disproportionate directly from the thalamus. It Within the overall population of somatotopic map of the therefore has access to the primary excitatory neurons, responses to contralateral body surface, descriptions of contact and a very few pads and to very large implying a general principle of pressure required to build numbers of pads were more coding by location [2]. Tuning for a description of tactile objects. common than responses to frequency of vibrotactile stimuli, or However, SII lacks the clear intermediate numbers. The former orientation of static stimuli has one-to-one somatotopic neurons might represent a specific also been reported [3]. However, organisation characteristic of SI. point of contact from a small the link between these basic SII neurons have large, even object, while the latter neurons dimensions of tactile sensation and bilateral receptive fields [6], would respond whenever an object Dispatch R885 was gripped by the whole hand. When a neuron responded to touch AB C on multiple pads, these often formed a line along a single digit or across multiple digits, suggesting convergence of information about a single object touching the hand. A few neurons (5%) showed excitatory responses to touch on some pads, but inhibitory responses to touch on others. The receptive field shape of these neurons typically shows a single zone of excitation, and a single zone of inhibition, often with an unresponsive zone in between. These neurons would presumably therefore give a maximal response to a single tactile object partially covering the finger surfaces. Such neurons could code specific Current Biology orientation of a large object within the hand (Figure 1A). The same Figure 1. Three forms of orientation selectivity in secondary somatosensory cortex. coding could be achieved by The lower row shows digit pads which excite (red) or inhibit (blue) the firing of a cortical combining the signals from neuron. (A) A neuron with both excitatory and inhibitory regions within its receptive inhibitory and excitatory neurons field. The tactile shape to which the neuron optimally responds is shown in blue in with complementary receptive the upper panel. (B) Signals from two neurons with purely excitatory and purely inhib- itory responses in complementary regions of the fingerpads could be integrated by fields: a hypothetical example is a higher order neuron to give the same selectivity for shape. (C) A neuron whose re- shown in panel B. Fitzgerald et al. sponse varies with the orientation of a stimulating bar. The optimal orientation on [5] do not discuss the connectivity each pad within the receptive field is shown. An optimal stimulus for this neuron would between different classes of SII be an object with the same gross orientation as A, but with additional oriented struc- neurons, but it seems possible that ture, such as corrugations. the excitatory-inhibitory neurons could integrate the information as edge detectors. Neurons edge of a small tactile object, provided by multiple lower-order responding to different orientations irrespective of the point of contact. excitatory and inhibitory neurons. on different digits could detect This might be a first step in a This convergence could also corners of objects. Behavioural transformation between a explain why mixed neurons were studies of active touch in human ‘skin-centred’ and an found less frequently than purely subjects suggest that a object-centred representation of excitatory or inhibitory neurons. In description of a tactile object touch, just as transformation general, the shape of SII receptive in terms of these geometric between viewer-centred and fields may allow representation of primitives could underlie the viewpoint-independent visual object orientation at large spatial ability to recognise objects by representations is considered scales. touch [1]. a first step in visual object Fitzgerald et al. [4] found that recognition [7]. Orientation Tuning 29% of neurons in SII showed A further question concerns how The first paper [4] focuses on the significant orientation tuning. They the neurons in different areas subset of neurons that modulated then compared the orientation of the somatosensory pathway their firing rate with the orientation tuning profiles of each neuron successively build the of the bar. It therefore deals with when the stimulus is delivered to representation of tactile shape. representation of orientation at different finger pads. A typical This might be answered by smaller spatial scales, within neuron (Figure 1C) might show comparing tuning properties of a single fingerpad. The authors significant orientation tuning on populations of neurons recorded at asked whether the orientation some pads, plus an untuned different locations along the tuning is common across multiple response or no response on pathway. If SII subserves tactile pads, or whether it differs across others. The preferred orientations shape computations, one might pads in a systematic way. The of the tuned pads tended to be expect a greater proportion of answers to these questions similar. That is, orientation neurons tuned for orientation would clearly advance an preferences were consistent there than in SI. However, understanding of tactile across pads with a single finger, studies of SI have yielded very integration: neurons with and also across fingers. This different estimates for the a common orientation preference arrangement could allow prevalence of orientation tuning, across several digits could act integration of information about the from 1–75%, so the relative Current Biology Vol 16 No 20 R886 importance of orientation evidence on this point seems fairly respectively [9]. However, many selectivity at different points along thin. Most classes of neuron were cells in area 5 and in SII respond to the somatosensory pathway found in all three cortical fields. either class of input [10,11]. remains unclear. The most convincing difference Body-referencing is an important between fields was the prevalence but relatively neglected aspect of Limitations and Future Directions of neurons responding to one or touch, which has no direct Taken together, these two papers a very few pads posteriorly. In the parallel in distance senses such [4,5] represent a valuable central and anterior fields, in as vision or hearing. It reminds contribution to identifying the contrast, neurons with very large us that the brain needs a model primitive elements of tactile receptive fields were much more of the perceiving self in order to shape representation in the common. The posterior field of SII form correct perceptual somatosensory system. The may therefore represent local representations of the outside results fit well with the properties of information about individual point world. neurons in earlier somatosensory contacts. Convergence of areas such as SI, and with several neurons carrying local References 1. Lederman, S.J., and Klatzky, R. (1993). computational theories of the information onto a single Extracting object properties through geometric information required for higher-order neuron might produce haptic exploration. Acta Psychol. 84, 29–40. object recognition. However, the the more extensive receptive 2. Penfield, W., and Rasmussen, T. (1950). authors themselves recognise fields of the central and anterior The Cerebral Cortex of Man. A Clinical two important methodological fields. The differences in Study of Localization of Function (New York, NY: MacMillan). limitations. orientation tuning between the 3. Mountcastle, V.B., Talbot, W.H., First, the apparatus used here three cortical fields provide Darian-Smith, I., and Kornhuber, H.H. (1967). Neural basis of the sense of applied the tactile stimulus to only a further paradox. Orientation- flutter-vibration. Science 155, one fingerpad at a time. What selective neurons were twice as 597–600. would happen if an oriented common in the central SII field as in 4. Fitzgerald, P.J., Lane, J.W., Thakur, P.H., and Hsiao, S.S. (2006). stimulus, such as the large the other two fields. However, their Receptive field (RF) properties of the corrugated object in Figure 1C, tuning was less sharp than that macaque second somatosensory cortex: RF size, shape, and somatotopic were placed simultaneously on all of neurons in the other two fields. organization. J. Neurosci. 26, the responsive finger pads? If The evidence for a gradient of 6485–6495. these neurons perform tactile shape-selectivity within SII is not 5. Fitzgerald, P.J., Lane, J.W., Thakur, P.H., and Hsiao, S.S. (2006). Receptive integration, the response to yet compelling. field properties of the macaque multiple preferred stimuli should be Finally, in the present second somatosensory cortex: representation of orientation on greater than the response to experiments, the monkeys were different finger pads. J. Neurosci. 26, a single preferred stimulus. trained to keep their hand still in 6473–6484. However, the summation a fixed position while stimuli were 6. Iwamura, Y. (2000). Bilateral receptive field neurons and callosal connections behaviour of these neurons has delivered. Because the hand was in the somatosensory cortex. Philos. not been systematically studied. still, touch at a given skin location Trans. R. Soc. Lond. B 355, 267–273. Similarly, the summation ability directly specified the presence 7. Marr, D. (1982). Vision (New York, NY: of untuned neurons (Figure 1B), of a tactile object at the W.H. Freeman and Company). when a single object covers corresponding spatial location. 8. de Vignemont, F., Haggard, P., and Ehrsson, H.H. (2005). Bodily illusions several pads, is not known. However, the fingers and hand modulate tactile perception. Curr. Biol. Second, the tactile stimulation in normally move when we interact 15, 1286–1290. 9. Mima, T., Ikeda, A., Terada, K., these studies was applied to the with objects in the world. Yazawa, S., Mikuni, N., Kunieda, T., passive hand, and was not Therefore, computing the shape of Taki, W., Kimura, J., and Shibasaki, H. behaviourally relevant to the a tactile object requires additional (1997). Modality-specific organization for cutaneous and proprioceptive sense animal. Tactile perception outside proprioceptive information about in human primary sensory cortex the laboratory almost always where the different contact points studied by chronic epicortical recording. Electroencephalogr. Clin. Neurophysiol. involves interaction with the object, are located in space relative to one 104, 103–107. and thus active touch. However, another. Put another way, touch 10. Kay, W.A., and Crammond, D. (1987). well-controlled psychophysical must be referenced to the body. Neuronal correlates in posterior parietal lobe of the expectation of events. Behav. experiments using active touch are De Vignemont et al. [8] showed that Brain Res. 24, 167–179. not easy, because the interaction perception of distance between 11. Fitzgerald, P.J., Lane, J.W., Thakur, P.H., and Hsiao, S.S. (2004). Receptive with the object depends on the two tactile contacts was rapidly field properties of the macaque subject’s exploratory strategy, altered by proprioceptive illusions second somatosensory cortex: and therefore cannot be of body shape induced by vibrating evidence for multiple functional representations. J. Neurosci. 24, controlled. the biceps tendon. This nicely 11193–11204. A third limitation concerns the demonstrates that higher tactile chain of processing within SII. In perception uses an internal Institute of Cognitive Neuroscience and both papers [4,5], the results from model of the body’s geometry. Department of Psychology, University the anterior, central and posterior Proprioceptive and cutaneous College London, 17 Queen Square, fields within SII are analysed information are processed London WC1N 3AR, UK. E-mail: [email protected] separately, as if the authors were separately in primary looking for a progression or somatosensory cortex, in areas 2 hierarchy of representations. The and 3a, versus 1 and 3b, DOI: 10.1016/j.cub.2006.09.024