Elsevier

NeuroImage

Volume 39, Issue 1, 1 January 2008, Pages 40-51
NeuroImage

Reproducible activation in BA2, 1 and 3b associated with texture discrimination in healthy volunteers over time

https://doi.org/10.1016/j.neuroimage.2007.08.026Get rights and content

Abstract

We aimed to quantify specific location and reproducibility of brain activation associated with discrimination of a moving textured surface in adult healthy volunteers over a 6-month interval. A sensory stimulation device was developed to provide a texture stimulus to the fingertips at a controlled speed and pressure. Repeat measurements of regional cerebral blood flow, using positron emission tomography (PET), were obtained in 10 healthy individuals, aged 33 to 80 years (mean = 55.8 years), at scanning sessions separated by 6 months. Stimulation and rest conditions were presented to either the right, dominant (n = 5) or left non-dominant (n = 5) hand. Activation location was objectively quantified with reference to probabilistic cytoarchitectonic maps. Differences in activation over time and regions of common activation were also quantified. Participants consistently activated Brodmann areas (BA) 2, 3b and 1, somatosensory areas of postcentral gyrus, at initial and 6-month studies: 93.1% of common activation for the right-hand (RH) and 60.6% for left-hand (LH) stimulation group were in these areas. Reproducible activation in BA6, 4a and 4p was also observed for the RH group (6.8% of common activation) and LH group (39.4%). There were no sites of significant difference over time for either hand. Highly consistent location of activation over time suggests that changes in loci of activation may be confidently monitored in adults using this paradigm. Use of probabilistic cytoarchitectonic maps permitted objective quantification of the anatomical location of the core of reproducible activation.

Introduction

Increasing evidence of change in sites of activation associated with recovery after stroke (Calautti and Baron, 2003) highlights the importance of longitudinal studies and reproducible paradigms. Despite the high prevalence of somatosensory loss after stroke and its impact on function (Carey, 1995, Kim and Choi-Kwon, 1996), there are relatively few neuroimaging studies of recovery of this ability (Weder et al., 1994, Cramer et al., 2000, Carey et al., 2002, Staines et al., 2002). Moreover there are very few investigations of the reproducibility of activation associated with sensory stimulation in healthy participants (Yetkin et al., 1996, Loubinoux et al., 2001). The value of longitudinal studies of recovery relies on objective, quantitative localization of specific sites of activation and reproducible methods. A sensory paradigm that is reproducible over an extended period of time, provides controlled stimulation and is able to be used with stroke patients is required. Here we investigated the reproducibility of activation during perception of a controlled touch stimulus in a sample of adult healthy volunteers, whose ages span the range of stroke survivors, over a 6-month time interval. Location of activation was objectively quantified using probabilistic cytoarchitectonic maps (Eickhoff et al., 2005).

Findings vary in relation to the reproducibility of cerebral activation even for simple motor and somatosensory tasks. While location (e.g. centroid) of activation appears to be reproducible in healthy volunteers (Schlaug et al., 1994, Yetkin et al., 1996, Carey et al., 2000, Loubinoux et al., 2001), extent and amplitude of signal response shows more variation (Schlaug et al., 1994, Cohen and DuBois, 1999, Shaw et al., 2003, van Gelderen et al., 2005), with a test–retest effect reported in some motor studies (Loubinoux et al., 2001). Variation in signal intensity and extent of activation was particularly evident between sessions separated by hours and months using functional magnetic resonance imaging (fMRI) (Cohen and DuBois, 1999, Loubinoux et al., 2001). In comparison, within session reproducibility was high (Loubinoux et al., 2001). Interestingly, after more extended intervals, changes were partially reversed (Loubinoux et al., 2001).

Accurate anatomical localization and delineation of component regions of brain activation are important in the characterization of activation. Typically functional imaging data are interpreted relative to stereotactic coordinates or macroanatomical landmarks (Eickhoff et al., 2005). Use of Talairach ‘labels’ is common but is limited as it does not provide information with respect to the inter-individual variability of the cytoarchitectonic areas (Geyer et al., 1999) or the relative probabilities for different cortical areas at a given location (Eickhoff et al., 2005). This is despite evidence of variable association between microstructural areas and macrostructural landmarks (Geyer et al., 1999, Grefkes et al., 2001, Zilles et al., 2002). Probabilistic cytoarchitectonic maps that provide stereotaxic information on the location and variability of cortical areas in the Montreal Neurological Institute (MNI) reference space have recently been made available for use through the ‘SPM Anatomy toolbox’ (Eickhoff et al., 2005). Importantly, the correspondence between functional activation data and anatomical brain structures can be quantified using these maps. Maps have been described in detail for primary and secondary somatosensory areas, regions of particular interest to the interpretation of our tactile paradigm. We therefore sought to use this new tool to objectively and quantitatively characterize the location of reproducible activation within primary and secondary somatosensory cortices.

Neuroimaging studies of brain activation associated with somatosensation in humans have involved a range of tasks from passive electrical nerve stimulation (Ibañez et al., 1995), cutaneous vibratory stimulation (Burton et al., 1993), passive touch using air puffs (Puce, 1995), brushing, stroking and scratching stimuli (Hammeke et al., 1994, Yetkin et al., 1995), through to active discrimination of objects using haptic touch and motor exploration (Seitz et al., 1991, Ledberg et al., 1995, Roland et al., 1998, Stoeckel et al., 2004, Young et al., 2004). In the tactile domain, discrimination of textured surfaces is a sensory-perceptual task that is important functionally, is commonly and characteristically impaired after stroke (Carey, 1995) and is considered by some to be the ‘prime province of touch’ (Taylor et al., 1973). A few have used embossed dot patterns or plastic gratings (Lin et al., 1996, Burton et al., 1997, Van Boven et al., 2005) to explore this modality in the functional imaging environment.

We have developed a sensory stimulation device that involves presentation of an embossed textured grid to the fingertips at a controlled speed and pressure (Carey et al., 2002). Importantly relative motion between skin and surface is achieved while not requiring active movement. Relative motion between the skin and surface is critical for the perception of texture (Lederman and Klatzky, 1987), whether the fingertip is the active mover or held stationary with the surface moving (Srinivasan et al., 1990, Vega-Bermudez et al., 1991). Thus, the paradigm has ecological validity while not being confounded by movement, which would confound investigation of the somatosensory system and may be problematic following stroke. Moreover, the texture grid used has strong theoretical and empirical foundations in monkey (Darian-Smith and Oke, 1980) and human (Morley et al., 1983) studies and is the same as that used in a clinical test of texture discrimination developed for use after stroke (Carey et al., 1997). The stimuli thus has the advantage of being related to a behavioral measure of sensation that has demonstrated validity and retest reliability and is not confounded by movement deficits.

Longitudinal studies of recovery poststroke demand reproducible paradigms and quantification of normal variability over time (Carey et al., 2000, van Gelderen et al., 2005). Moreover, the probability of location of activation in a specific region needs to be quantified, even in small samples, as is often the case in patient studies. Our purpose was to establish the reproducibility over time of activation associated with perception of a moving textured stimulus as delivered by our novel device and to quantify the location of this activation using recently available probabilistic cytoarchitectonic maps (Eickhoff et al., 2005). We hypothesized that there would be no significant difference in activation over a 6-month interval in our group of adult healthy volunteers of stroke-related age and that the reproducible core of activation would be located in the primary somatosensory cortex contralateral to the hand stimulated.

Section snippets

Participants

Ten healthy volunteers with no history of neurological or sensory impairment were recruited to the study. Ages ranged from 33 to 80 (mean age 55.8, SD 14.6 years). All were right-hand dominant (Oldfield, 1971). All had normal magnetic resonance (MR) brain images, as reported by a clinical radiologist. The study was approved by local hospital and university human ethics and radiation committees. All experimental procedures were conducted in accordance with the hospital and University Human

Background characteristics and sensory thresholds

Background details and sensory thresholds of healthy volunteers are reported in Table 1. All subjects showed sensory thresholds within normal range for both hands for the Tactile Discrimination Test (Carey et al., 1997). Moreover, all were able to clearly feel the stimulus and concentrated on the task, as indicated by the VAS obtained immediately after the scan. The ability to feel the stimulus was perceived to be high (mean 9.68/10 at the initial and 9.69/10 at 6-month study) and did not

Discussion

Reproducible activation, associated with a controlled tactile stimulation task, was observed in somatosensory regions BA2, 3b and 1 contralateral to the stimulated hand, as characterized relative to cytoarchitectonic probabilistic maps (Eickhoff et al., 2005) in a group of adult healthy volunteers spanning the age range of people who may experience a stroke. There were no significant differences in activation maps over the 6-month interval for either the RH or LH stimulation groups. Moreover,

Conclusion and recommendations

In summary, new evidence of a core of reproducible activation in BA2, 1 and 3b indicates that the tactile stimulation paradigm may be confidently used to probe the somatosensory system and localize cortical activity in response to somatosensory stimulation. Strong convergence of findings with other tactile imaging studies and with expected regions of activation provides further support for this paradigm. While the power of this study was low to detect differences, it was adequate to define a

Acknowledgments

We wish to thank participants for their involvement in the study and the staff at the Centre for PET, Austin Health. This research was supported by the National Health and Medical Research Council (NHMRC) of Australia and the National Stroke Research Institute. Dr. Carey is supported by an NHMRC Career Development Award (grant no 307905) and Dr. Egan by an NHMRC Principal Research Fellowship (grant no 400317). We would particularly like to thank Dr. Simon Eickhoff for his guidance and advice

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