Two Distinct Ipsilateral Cortical Representations for Individuated Finger Movements

Cerebral Cortex June 2013;23:1362–1377 doi:10.1093/cercor/bhs120 Advance Access publication May 17, 2012 Two Distinct Ipsilateral Cortical Representations for Individuated Finger Movements Jörn Diedrichsen1, Tobias Wiestler1 and John W. Krakauer2,3 1 Institute of Cognitive Neuroscience, University College London, London, UK 2Department of Neurology and 3Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21287, USA Address correspondence to Jörn Diedrichsen, Institute of Cognitive Neuroscience, University College London, Alexandra House, 17 Queen Square, London WC1N 3AR, UK. Email: . Keywords: cortical representation, fMRI, motor cortex, multivoxel pattern analysis Introduction Finger movements appear to be (almost) exclusively controlled by cortical areas in the contralateral hemisphere—if control is defined as a direct connection to the spinal cord (Brinkman and Kuypers 1973; Soteropoulos et al. 2011). However, many cortical motor areas also show overall activity increases or decreases in relation to finger movements of the ipsilateral hand (Kim et al. 1994; Cramer et al. 1999; Hanakawa et al. 2005; Verstynen et al. 2005; Talelli, Waddingham et al. 2008; Horenstein et al. 2009). The functional role of these ipsilateral cortical changes remains unclear. An important first step in answering this question is to determine whether and how characteristics of ipsilateral actions are encoded in cortical circuits. This is based on the premise that a region that is involved in the control of movement, possibly through modulation of the other hemisphere, should contain neurons that are differentially active with respect to the relevant control variable. In other words, a region should contain a representation for the task control variable as a necessary (if not sufficient) condition for a region to play a functional role in control of this variable. For example, neurons in the hand area of the primary motor cortex show a differential tuning for different finger movements of the contralateral hand. Even though individual neurons respond to presses of multiple fingers (Schieber 2002; Acharya et al. 2008), and activation patches for individuated fingers overlap greatly (Indovina and Sanes 2001; Wiestler et al. 2011), the neuronal population as a whole encodes the exact action very precisely. In contrast, an area that shows exactly the same neuronal firing pattern regardless of the digit involved cannot play either a direct (cortico-spinal projections) or indirect (cortico-cortical modulation) role in “control” of individuated finger movements, but can at best have a supportive function, such as sustaining attention to the task or controlling postural muscles in a finger-invariant manner. Although the primary motor cortex appears to represent the movement direction of the ipsilateral arm (Donchin et al. 1998; Ganguly et al. 2009), there is currently no evidence for an analogous ipsilateral representation of individuated finger movements. Using high-resolution functional magnetic resonance imaging (fMRI) and a statistical approach that tests for representation rather than average activation, we characterized how cortical motor areas represent ipsilateral isometric finger presses. If neurons are activated differentially for each finger, and if neuronal populations with similar properties are sufficiently clustered together, then we should be able to decode individual fingers from local fMRI activity patterns. Using this decoding approach, called multivoxel pattern analysis (MVPA, Kriegeskorte et al. 2006), we have recently found finger representations in the primary motor cortex and the cerebellum. It is noteworthy that this method, unlike a center-of-gravity (COG) analysis of individual fingers (Indovina and Sanes 2001), does not require any systematic somatotopy. Indeed, using this method, we were able to show finger representations in the inferior cerebellum, which lack any discernable somatotopic organization for individual fingers (Wiestler et al. 2011). The experiments reported here show that there are 2 fundamentally different types of representation of ipsilateral fingers. During unimanual presses (Experiment 1), we find that the activity patterns elicited by each ipsilateral finger are highly correlated with those for the corresponding contralateral finger. Furthermore, these mirrored activation patterns disappear during bimanual finger presses (Experiment 2). Therefore, we conclude that ipsilateral representations during unimanual actions rely on the activation of the very same neuronal circuits that control the mirror-symmetric contralateral action. That is, if the 2 representations were at least partially independent, the region would have been able to represent both the ipsi- and contralateral actions simultaneously. A second type of ipsilateral representation becomes visible during bimanual actions. Here, both a premotor region and a parietal region encode unique © The Authors 2012. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Movements of the upper limb are controlled mostly through the contralateral hemisphere. Although overall activity changes in the ipsilateral motor cortex have been reported, their functional significance remains unclear. Using human functional imaging, we analyzed neural finger representations by studying differences in finegrained activation patterns for single isometric finger presses. We demonstrate that cortical motor areas encode ipsilateral movements in 2 fundamentally different ways. During unimanual ipsilateral finger presses, primary sensory and motor cortices show, underneath global suppression, finger-specific activity patterns that are nearly identical to those elicited by contralateral mirror-symmetric action. This component vanishes when both motor cortices are functionally engaged during bimanual actions. We suggest that the ipsilateral representation present during unimanual presses arises because otherwise functionally idle circuits are driven by input from the opposite hemisphere. A second type of representation becomes evident in caudal premotor and anterior parietal cortices during bimanual actions. In these regions, ipsilateral actions are represented as nonlinear modulation of activity patterns related to contralateral actions, an encoding scheme that may provide the neural substrate for coordinating bimanual movements. We conclude that ipsilateral cortical representations change their informational content and functional role, depending on the behavioral context. combinations of contra- and ipsilateral fingers. This type of representation is ideally suited to learning and controlling coordinated bimanual actions. Materials and Methods (...truncated)