The areas of the brain that receive inputs from our senses have a map-like structure. In an area called the visual cortex this map represents our field of vision; in the auditory cortex, it represents the range of different tones we can hear. The sense of touch is processed in the somatosensory cortex: an area of the brain that is organised around a map of the body, with adjacent regions of the cortex representing adjacent regions of the body. The clear structure of these brain regions makes them ideal for exploring how the organisation of the brain changes over time.

How quickly can changes to the touch inputs that the brain receives cause the map in the somatosensory cortex to reorganise? Can these effects be produced in just 24 hours? And would this remapping affect how we perceive touch? To investigate these questions, Kolasinski et al. glued together the right index and right middle fingers of healthy human volunteers. This separated the middle and ring fingers: a pair that usually move together due to the anatomical structure of the hand.

Functional magnetic resonance imaging of the brain’s activity revealed that within 24 hours of the gluing, the brain’s representation of the ring finger moved away from that of the middle finger, and towards the representation of the little finger. A perceptual judgment task mirrored this finding: after 24 hours of gluing, the participants became better at distinguishing between the middle and ring fingers and worse at distinguishing between the ring and little fingers. This is a powerful demonstration of the human brain’s potential to adapt and reorganise rapidly to changes to sensory inputs.

The sense of touch declines gradually with age and may also be reduced as a result of disease such as stroke. A long-term challenge is to understand how the sensory regions of the brain change during this loss of sensation. Further research could then investigate how to maintain the structure of the cortical map to prolong or restore high quality touch sensation.

Evidence for experience-dependent plasticity in the adult mammalian brain exists across a variety of sensory modalities (Fu and Zuo, 2011). The ordered somatotopy of primary somatosensory cortex (SI) has long served as a model system for studies of cortical reorganisation, with a wealth of evidence from both the non-human primate and rodent literature linking both extreme and subtle peripheral changes in somatosensory inputs over months or years to alterations in cortical maps (Buonomano and Merzenich, 1998; Feldman and Brecht, 2005).

In the human brain, there has also been evidence of experience-dependent remapping in SI. Considerable emphasis has been placed upon cross-sectional differences in the cortical organisation of SI observed in specialist populations, such as musicians, or patients with sensorimotor dysfunction, such as focal dystonia (Elbert et al., 1995; Bara-Jimenez et al., 1998; Nelson et al., 2009; Kalisch et al., 2009). However, only limited longitudinal evidence exists that directly demonstrates remapping at the level of human SI, either in response to altered hand usage patterns (Stavrinou et al., 2007) or more intensive Hebbian co-activation paradigms delivering specific patterns of tactile stimulation to the fingertips (Pleger et al., 2001, 2003; Hodzic et al., 2004; Vidyasagar et al., 2014). There remains a limited understanding of the speed of SI plasticity and how cortical changes relate to behaviour. Here we address this gap in the literature, investigating the propensity for rapid experience-dependent cortical reorganisation and the behavioural relevance thereof.

Using a well-validated paradigm of single-subject fMRI mapping of human SI at 7 tesla (Sanchez-Panchuelo et al., 2010; Kolasinski et al., 2016), we asked two questions. First, can experience-dependent plastic remapping of SI somatotopy be elicited in the human cortex in just 24 hr? Second, are any observed cortical changes reflected in altered tactile function? A complementary combination of fMRI and behavioural psychophysics were used to investigate the effect of a 24 hr manipulation in which the right index (D2) and right middle digit (D3) were joined together using skin glue. Based on the primate literature (Clark et al., 1988; Allard et al., 1991), we hypothesised that forced co-use of the glued digit pair would result in increased tactile co-activation across the digits, and an increase in their shared cortical representation. An alternative hypothesis posited that compensatory behaviour during the 24 hr gluing manipulation would promote changes in the cortical representations of adjacent, but unaffected digits.

In the fMRI cohort, SI digit somatotopy of the right hand was mapped at 7 tesla (Kolasinski et al., 2016) after two periods of normal hand use (control 1 and control 2), and after the gluing manipulation. In each session, fMRI data were acquired during a block design task and phase-encoding task. We first asked whether the amount of cortical overlap between digit representations in SI changed after the gluing manipulation in comparison with two control sessions using the phase-encoding fMRI data. Measures of inter-digit overlap were calculated for adjacent digit pairs (D2-D3: index-middle, D3-D4: middle-ring, D4-D5: ring-little; Figure 1A). A two-way repeated measures ANOVA indicated a significant interaction between session and digit pair on the amount of cortical overlap (F_(4,32) = 13.412, p<0.0005, η²:0.626) (Figure 1B). This was driven by a significant reduction in the cortical overlap between D3-D4 (Simple main effect: F_(2,16) = 23.379, p<0.0005; Pairwise Sidak-corrected p<0.05) and a significant increase in the overlap of D4-D5 (Simple main effect: F_(2,16) = 13.384, p<0.0005; Pairwise Sidak-corrected p<0.05) in the glued condition compared with both control sessions (Figure 1B). No significant change was found in the overlap between D2 and D3, the glued digits, where changes have been observed in similar but longer term studies in non-human primates (Clark et al., 1988; Allard et al., 1991). No shift in peak-to-peak distance between the digit representations (Supplementary file 1) or the overall surface area of each digit representation was observed (Figure 1—figure supplement 1). No systematic difference in the fit between the phase-encoding models and fMRI signal were observed across sessions (Supplementary file 2).

Figure 1 with 3 supplements see all

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Figure 1—source data 1

Data presented in Figure 1B.

DICE coefficients representing digit overlap for three digit pairs (D2–D3, D3–D4 and D4–D5) across three conditions (Control 1, Control 2 and Glued).

https://doi.org/10.7554/eLife.17280.004

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To further explore the observed change in inter-digit overlap with no change in overall cortical surface area of each digit representation, the fMRI representations of digit 4 used to calculate the cortical overlap metrics (Dice coefficients) were visualised for each participant and session (Figure 2). This data revealed that the observed changes presented in Figure 1B were driven by an expansion in the representation of digit 4 adjacent to digit 5 and a corresponding contraction at the boundary with digit 3.

Figure 2

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Representational similarity analysis conducted on the block design fMRI data also implicated changes in the representation of digit 4 (Figure 3). These data demonstrated a shift in the representation of D4 away from D3 and towards D5.

Figure 3

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Figure 3—source data 1

Data presented Figure 3A.

Representational similarity analysis distance metrics for adjacent digit pairs (D2–D3, D3–D4 and D4–D5) across three conditions (Control 1, Control 2 and Glued).

https://doi.org/10.7554/eLife.17280.010

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Given the fMRI data were strongly suggestive of changes in cortical overlap outside of the glued digit pair (D2-D3), we sought to more fully investigate the observed pattern of short-term reorganisation by assessing the behavioural correlates of the gluing manipulation. The same experimental design and gluing manipulation were applied in a separate cohort. Instead of an fMRI scan, nine participants undertook behavioural psychophysics tasks during each session. The first task involved temporal order judgment (TOJ), where pairs of rapid vibrotactile stimuli were applied to adjacent digit pairs of the right hand at varying interstimulus intervals. Participants judged which digit was stimulated first. A psychometric function was fitted to the resulting accuracy data, from which a metric of tactile discrimination ability was calculated for each adjacent digit pair (Just Noticeable Difference: JND). Greater values of JND are associated with poorer discrimination across an adjacent digit pair (Figure 4A). We asked whether the ability to distinguish the order of two stimuli delivered in rapid succession, one each on two adjacent digits, differed in the session directly following the gluing manipulation in comparison with the control sessions.

Figure 4 with 1 supplement see all

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Figure 4—source data 1

Data presented Figure 4B.

Just Noticeable Difference (JND) values representing tactile discrimination ability for three digit pairs (D2–D3, D3–D4 and D4–D5) across three conditions (Control 1, Control 2 and Glued).

https://doi.org/10.7554/eLife.17280.012

Download elife-17280-fig4-data1-v2.csv

Figure 4—source data 2

Data presented Figure 4—figure supplement 1B.

Frequency of mis-localisations for motor confusion task across adjacent digit pairs (D2–D3, D3–D4 and D4–D5) across three conditions (Control 1, Control 2 and Glued).

https://doi.org/10.7554/eLife.17280.013

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We generated behavioural predictions based on our fMRI findings of altered cortical maps after the gluing manipulation (Figure 3). Specifically, we hypothesised that the gluing manipulation would result in improved tactile discrimination (reduced JND) across D3-D4, which demonstrates reduced cortical overlap, and diminished tactile discrimination (increased JND) across D4-D5, which demonstrates increased cortical overlap. Data from eight participants met the goodness of fit threshold for all sessions (R² > 0.4). A two-way repeated measures ANOVA indicated a significant interaction between session and digit pair on tactile discrimination (JND) (F_(4,28) = 14.613, p<0.0005, η²:0.676). This was driven by a significant reduction in JND across D3-D4 (Simple main effect: F_(2,14) = 14.631, p<0.0005; Pairwise Sidak-corrected p<0.05), and a significant increase in the JND across D4-D5 (Simple main effect: F_(2,14) = 10.578, p=0.002; Pairwise Sidak-corrected p<0.05) in the gluing condition compared with both control sessions (Figure 4B). No significant change in tactile discrimination was found for D2-D3, the glued digits. In other words, after the gluing manipulation, tactile discrimination was improved across D3-D4 and was diminished across D4-D5, with no change in the glued digits D2-D3. This finding was supported by similar results from a second task, assessing motor confusion, which involved rapidly cued button presses using individual digits. There was an increase in the level of confusion between digits 4 and 5 after the gluing manipulation compared with the control conditions (Figure 4—figure supplement 1).

The fMRI and psychophysics results present complementary evidence for functionally relevant reorganisation in human SI following just a 24 hr peripheral change in hand use. Previous longitudinal studies of detailed somatotopic remapping in humans using MEG or standard resolution fMRI have provided evidence for a general change in the distance between digit representations (Stavrinou et al., 2007; Mogilner et al., 1993), or a synchronisation in activity pattern of non-adjacent digits (Vidyasagar et al., 2014) after coupled stimulation across digits. Conversely, an intervention involving hand and arm immobilisation drove diminished tactile acuity and a corresponding reduction in BOLD activity in contralateral SI (Lissek et al., 2009). Our results build on this work, demonstrating that usage-dependent changes in the overlap of SI digit representations are associated with a corresponding change in the ability to differentiate tactile inputs to the digits. Specifically, an increase in the cortical overlap between D4 and D5 was accompanied by a reduction in the tactile discrimination ability across these two digits.

A consistent feature of our findings was that cortical reorganisation and behavioural change was not observed for the glued digit pair (D2-D3). Instead, we saw changes in cortical overlap, and corresponding change in behavioural performance, for the other digit pairs. Specifically, we saw a shift of D4 away from D3 and towards D5. These findings reject our hypothesis of increased tactile synchronisation driving an increase in cortical overlap. Instead, these data support the alternative hypothesis that compensatory behaviour in other digits during the 24 hr manipulation drives off-target effects.

In light of the considerable dexterous abilities specific to the human hand (Young, 2003) and the short duration of the gluing manipulation, it is feasible that the observed remapping reflects compensatory behavioural changes in the pattern of hand use during the manipulation. Rather than learning to coordinate and co-use the glued digits, participants may have adapted synergies with the non-manipulated digits. In this case, the increased physical separation of D3 and D4 during the gluing reduces the usually high degree of anatomical enslavement seen peripherally between these two digits (Kim et al., 2008), freeing D4 to function even more synergistically with D5. This argument is supported by the observed pattern of increased motor confusion between digits 4 and 5 after the gluing manipulation (Figure 4—figure supplement 1), demonstrating potential changes in movement synergies, that may explain the somatosensory changes observed. This finding complements recent observations that patterns of synergistic digit usage are strongly reflected in the generalisation of tactile learning from trained to adjacent untrained digits (Dempsey-Jones et al., 2016).

The two fMRI datasets showed independent evidence of a shift in the digit 4 representation during the gluing manipulation: away from digit 3, and towards digit 5 (Figures 1 and 3), raising questions regarding the underlying mechanism driving this reorganisation. Similar studies undertaken over a period of months in non-human primates have reported the emergence of overlapping receptive fields in response to the fusion of two adjacent digits (Clark et al., 1988; Allard et al., 1991). The spatial resolution of BOLD fMRI is, of course, poorer than invasive mapping techniques. Nonetheless, it is possible that the observed changes in cortical activation could result from shifts in population receptive fields at the boundary of cortical digit representations (Besle et al., 2014), or even changes in multidigit receptive fields (Thakur et al., 2012). As well as reorganisation in the cortex, strong evidence also suggests considerable plastic potential in subcortical structures, which is mirrored in the cortex (Jones, 1996; Rausell et al., 1998; Kambi et al., 2014). The remapping observed in SI here may therefore result from reorganisation in lower level nuclei of the ascending somatosensory pathway.

A shift in the cortical representation of digit 4 (Figure 2), rather than an overall enlargement of the representation, distinguishes the observed pattern of cortical change from previous studies of artificial tactile co-activation, wherein a generalised cortical magnification of the manipulated digit is observed (Pleger et al., 2001, 2003; Hodzic et al., 2004). The cortical shift perhaps reflects how naturalistic behavioural changes in hand use are reflected in the cortex, with remapping based on functional need; in this case, leading to perceptual improvements in certain digit pairs (D3/D4), and worsening in others (D4/D5).

What mechanism drives the observed change in cortical overlap? In vivo studies in rodent barrel cortex demonstrate that a 24 hr period of altered sensory input can induce increases in synaptic density in the corresponding cortical representation (Knott et al., 2002). This could unmask or potentiate pre-existing divergent or silenced connections between adjacent digit representations (DeFelipe et al., 1986; Recanzone et al., 1992; Huntley, 1997). The question remains: how could this cortical shift occur with no associated change in the surface area or location of peak activation of the digit 4 representation? Patterns of local horizontal connectivity in the cortex are established during development and moulded throughout life (Sur and Rubenstein, 2005). Homeostatic mechanisms also exist to maintain balance in cortical activity (Turrigiano and Nelson, 2000), and to preserve the scaling and pattern of cortical topography (Sharma et al., 2000; Vanderhaeghen et al., 2000). It is plausible that the gluing manipulation results in the potentiation of excitatory horizontal connectivity between the representations of digits 4 and 5, and the concurrent weakening of connectivity between the representations of digits 3 and 4. After 24 hr, we observe the resulting pattern of cortical reorganisation (Figures 2 and 3), wherein the relative positions of the representations have changed, but features of the maps firmly established in development, remain in place. A comparable process of reduced inhibition prior to remapping has been reported in studies of sensory deprivation in rodent barrel cortex. Reduced inputs after whisker clipping produce a local pattern of cortical disinhibition and broadening excitation, followed by subsequent cortical contraction of the representation (Albieri et al., 2015). In this case, changes in the relative inputs across different digits may prompt a transient disinhibitory cortical milieu, and the subsequent re-establishment of modified excitatory networks within the cortex, wherein the cortical representations have shifted to reflect new usage patterns. The unmasking of latent excitatory connections prior to any homeostatic increase in lateral inhibition to rebalance cortical excitability could explain the observation of more marked changes in tactile perception and representational surface area after very short and intense tactile training interventions, or rTMS protocols (Pleger et al., 2003; Tegenthoff et al., 2005; Ragert et al., 2008; Dinse and Tegenthoff, 2015).

The consistent cortical changes at the flanks of the digit 4 representation (Figure 2) in the absence of changes in the location of peak activation suggest that the latter may not be the most informative feature of rapid map reorganisation. The existence of such hard-wired elements in cortical somatotopy is supported by evidence of SI constraining the extent of reorganisation within the somatosensory system: acting as a blueprint for lower level nuclei (Zembrzycki et al., 2013), enforcing some limits on plasticity, and potentially explaining the persistence of SI somatotopic features long after marked peripheral changes, such as amputation (Kikkert et al., 2016).

Given the increasingly recognised contribution of motor efference information to activity patterns in somatosensory cortex (Lee et al., 2008, 2013), it is also possible that changes in motor outputs over the course of 24 hr may shape patterns of SI activity, promoting a top-down form of SI experience-dependent plasticity.

The rapidity of cortical changes shown herein supports further investigation of rapid and targeted therapeutic interventions in conditions such as focal dystonia, where maladaptive changes in somatotopy have previously been reported (Bara-Jimenez et al., 1998). The mechanistic link between short-term plasticity and long-term circuit changes remains unclear (Holtmaat and Svoboda, 2009; Johansen-Berg et al., 2012). Therefore, further questions remain as to how short-term peripheral manipulations could be used to induce sustained modification or refinement of fine grain functional cortical organisation, as a means to enhance or rehabilitate tactile function.

All data were acquired in accordance with local central university research ethics committee approval (University of Oxford MSD-IDREC-C2-2013-05). Eighteen participants were recruited (age range 19–33 years, eight females; Supplementary file 3) and provided written informed consent. All participants were right handed according to the Edinburgh Handedness Inventory (Oldfield, 1971), had no history of neurological or psychiatric illness, and met local MRI safety criteria where appropriate.

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Author details

1. James Kolasinski

   1. Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
   2. University College, Oxford, United Kingdom

   Contribution

   JK, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   james.kolasinski@ndcn.ox.ac.uk

   Competing interests

   No competing interests declared.

   "This ORCID iD identifies the author of this article:" 0000-0002-1599-6440

2. Tamar R Makin

   1. Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
   2. Institute of Cognitive Neuroscience, University College London, London, United Kingdom

   Contribution

   TRM, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

   "This ORCID iD identifies the author of this article:" 0000-0002-5816-8979

3. John P Logan

   Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

   Contribution

   JPL, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

   "This ORCID iD identifies the author of this article:" 0000-0002-4469-2948

4. Saad Jbabdi

   Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

   Contribution

   SJ, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

5. Stuart Clare

   Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

   Contribution

   SC, Acquisition of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

6. Charlotte J Stagg

   1. Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
   2. Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, Oxford, United Kingdom

   Contribution

   CJS, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

7. Heidi Johansen-Berg

   Oxford Centre for fMRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

   Contribution

   HJ-B, Conception and design, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   HJ-B: Reviewing editor, eLife

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