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      Age-related changes in causal interactions between cortical motor regions during hand grip

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          Abstract

          Brain activity during motor performance becomes more widespread and less lateralized with advancing age in response to ongoing degenerative processes. In this study, we were interested in the mechanism by which this change in the pattern of activity supports motor performance with advancing age. We used both transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) to assess age related changes in motor system connectivity during isometric hand grip. Paired pulse TMS was used to measure the change in interhemispheric inhibition (IHI) from contralateral M1 (cM1) to ipsilateral M1 (iM1) during right hand grip. Dynamic Causal Modelling (DCM) of fMRI data was used to investigate the effect of age on causal interactions throughout the cortical motor network during right hand grip. Bayesian model selection was used to identify the causal model that best explained the data for all subjects. Firstly, we confirmed that the TMS and DCM measures both demonstrated a less inhibitory/more facilitatory influence of cM1 on iM1 during hand grip with advancing age. These values correlated with one another providing face validity for our DCM measures of connectivity. We found increasing reciprocal facilitatory influences with advancing age (i) between all ipsilateral cortical motor areas and (ii) between cortical motor areas of both hemispheres and iM1. There were no differences in the performance of our task with ageing suggesting that the ipsilateral cortical motor areas, in particular iM1, play a central role in maintaining performance levels with ageing through increasingly facilitatory cortico-cortical influences.

          Highlights

          ► DCM of fMRI data was used to investigate the effect of ageing on the motor network. ► The facilitatory influence of contra-to ipsilateral M1 increases with age. ► This is consistent with results from independently acquired neurophysiological data. ► Connections between ipsilateral motor regions were more facilitatory with ageing. ► These enhanced connections might help to maintain performance levels with ageing.

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          Dynamic causal modelling.

          L. Harrison, W. Penny, W Penny (2003)
          In this paper we present an approach to the identification of nonlinear input-state-output systems. By using a bilinear approximation to the dynamics of interactions among states, the parameters of the implicit causal model reduce to three sets. These comprise (1) parameters that mediate the influence of extrinsic inputs on the states, (2) parameters that mediate intrinsic coupling among the states, and (3) [bilinear] parameters that allow the inputs to modulate that coupling. Identification proceeds in a Bayesian framework given known, deterministic inputs and the observed responses of the system. We developed this approach for the analysis of effective connectivity using experimentally designed inputs and fMRI responses. In this context, the coupling parameters correspond to effective connectivity and the bilinear parameters reflect the changes in connectivity induced by inputs. The ensuing framework allows one to characterise fMRI experiments, conceptually, as an experimental manipulation of integration among brain regions (by contextual or trial-free inputs, like time or attentional set) that is revealed using evoked responses (to perturbations or trial-bound inputs, like stimuli). As with previous analyses of effective connectivity, the focus is on experimentally induced changes in coupling (cf., psychophysiologic interactions). However, unlike previous approaches in neuroimaging, the causal model ascribes responses to designed deterministic inputs, as opposed to treating inputs as unknown and stochastic.
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            Imaging the premotor areas.

            Nathalie Picard, Peter L Strick (2001)
            Recent imaging studies of motor function provide new insights into the organization of the premotor areas of the frontal lobe. The pre-supplementary motor area and the rostral portion of the dorsal premotor cortex, the 'pre-PMd', are, in many respects, more like prefrontal areas than motor areas. Recent data also suggest the existence of separate functional divisions in the rostral cingulate zone.
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              The origin of corticospinal projections from the premotor areas in the frontal lobe.

              RP Dum, PL Strick (1991)
              We determined the origin of corticospinal neurons in the frontal lobe. These neurons were labeled by retrograde transport of tracers after injections into either the dorsolateral funiculus at the second cervical segment or the gray matter of the spinal cord throughout the cervical enlargement. Using retrograde transport of tracer from the arm area of the primary motor cortex, we defined the arm representation in each premotor area in another set of animals. We found that corticospinal projections to cervical segments of the spinal cord originate from the primary motor cortex and from the 6 premotor areas in the frontal lobe. These are the same premotor areas that project directly to the arm area of the primary motor cortex. The premotor areas are located in parts of cytoarchitectonic area 6 on the lateral surface and medial wall of the hemisphere, as well as in subfields of areas 23 and 24 in the cingulate sulcus. The total number of corticospinal neurons in the arm representations of the premotor areas equals or exceeds the total number in the arm representation of the primary motor cortex. The premotor areas collectively comprise more than 60% of the cortical area in the frontal lobe that projects to the spinal cord. Like the primary motor cortex, each of the premotor areas contains local regions that have a high density of corticospinal neurons. These observations indicate that a substantial component of the corticospinal system originates from the premotor areas in the frontal lobe. Each of the premotor areas has direct access to the spinal cord, and as a consequence, each has the potential to influence the generation and control of movement independently of the primary motor cortex. These findings raise serious questions about the utility of viewing the primary motor cortex as the "upper motoneuron" or "final common pathway" for the central control of movement.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Neuroimage
                Journal ID (iso-abbrev): Neuroimage
                Title: Neuroimage
                Publisher: Academic Press
                ISSN (Print): 1053-8119
                ISSN (Electronic): 1095-9572
                Publication date PMC-release: 15 February 2012
                Publication date (Print): 15 February 2012
                Volume: 59
                Issue: 4-4
                Pages: 3398-3405
                Affiliations
                [a ]Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, London, UK
                [b ]Wellcome Trust Centre for NeuroImaging, UCL Institute of Neurology, London, UK
                Author notes
                [* ]Corresponding author at: Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, Box 146, 33 Queen Square, London, WC1N 3BG, UK. Fax: + 44 207 278 9836. m.boudrias@ 123456ucl.ac.uk
                Article
                Publisher ID: YNIMG8903
                DOI: 10.1016/j.neuroimage.2011.11.025
                PMC ID: 3315004
                PubMed ID: 22119651
                SO-VID: da65db9f-f2c0-47a5-97cf-71e8bf9ec5be
                Copyright © © 2012 Elsevier Inc.
                License:

                This document may be redistributed and reused, subject to certain conditions.

                History
                Date received : 24 August 2011
                Date revision received : 17 October 2011
                Date accepted : 4 November 2011
                Categories
                Subject: Article

                ScienceOpen disciplines: Neurosciences
                Keywords: dcm,ageing,fmri,motor system,connectivity
                Data availability:
                ScienceOpen disciplines: Neurosciences
                Keywords: dcm, ageing, fmri, motor system, connectivity

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