A goal of the rehabilitation professional is to help their patients learn the successful execution of movements. Verbal instruction is one means by which learning movement can occur. In recent years, literature on the effects of instruction and performance has investigated focus of attention effects. Substantial evidence supports the premise that focusing attention on a specific body part related to movement or on the skill itself can affect performance and learning.1–3 Instructional focus can be subdivided into an internal focus and an external focus of attention. An internal focus uses instruction to direct one’s focus to specific aspects of one’s body movement, whereas an external focus uses instruction to direct one’s focus toward the effects of his or her movement on the environment.4 For example, during balance-board training exercises, asking a participant to “focus on keeping their feet level” would be deemed an internal focus, whereas asking a participant to “focus on keeping the board level (ie, the effects of keeping their feet level)” would be an external focus.5 While the change in instruction is subtle, a comprehensive review demonstrated that an external focus facilitates enhanced performance and greater skill learning relative to an internal focus.3 One theoretical explanation for the skilled performance and learning changes resulting from an external focus is the constrained-action hypothesis.6–8 This theory suggests that an external focus reduces the level of conscious interference in control processes allowing the body to behave automatically, whereas an internal focus is thought to require more conscious control over control processes disrupting the execution of motor skills.
Relevant findings from the attentional focus research have called for a consideration in rehabilitation in which practitioners may consider the potential benefits of using an external focus of attention.9,10 For example, findings support that external focus facilitates safer biomechanics from an orthopedic injury perspective.11,12 With respect to instruction the addition of visual stimuli has been shown to enhance performance when used with an external focus,13 a technique that can easily be adopted in rehabilitation and sporting venues. The way we direct our attentional resources is considered the main mediator of cognition during visual searches.14 In addition, research suggests that vision mediates the relationship between attentional focus and performance.15 Therefore, integrating the visual stimuli with an external focus instruction would promote improved learning and performance.
A better understanding of the neural activity associated with attentional focus and motor skill may allow for more precise rehabilitation guidelines based on specific neural mechanisms. To date this has been done primarily using fine motor movements (key pressing tasks) due to the logistics of performing a gross motor movement using functional magnetic resonance imaging (fMRI). Zentgraf et al16 provided specific instructions to direct subjects’ attention internally (focus on their fingers when pressing the keys) or externally (focus on the keys being pressed). Results revealed that an external focus demonstrated a significantly higher blood oxygenation level dependent response in the primary motor cortex, somatosensory cortex, and insular region of the left hemisphere. The authors surmised from these regions that are associated with sensory function, that an external focus promoted task-adequate brain activity for movement execution by shifting focus toward exteroceptive information. However, it is important to clarify that these assumptions are speculative. The authors did not measure sensory function or assess participants’ cognitive states, nor report the neural activation and key pressing behavioral data association. Thus, limiting our combined understanding of how differing neural activation resulting from attentional focus drives behavior or reflects participants’ state of mind. Further, this work is limited by participants completing only fine motor movements, which are perceived as more cognitively demanding than gross motor movements,17 practicing the task prior to receiving attentional focus instruction, the possibility that instructions given during the practice task may have biased attentional control,18 and the brain data being obtained 1 day following training.
Given the lack of understanding of attentional focus and associated neural mechanisms during execution and learning of gross motor skills, the purpose of this study was to examine brain activation differences when participants performed a gross motor movement of the lower-extremity using an internal and external focus of attention. The integration of attentional focus instruction and neuroimaging during gross motor movement will help provide a mechanistic understanding for the effects of attentional focus for motor performance and learning. To better understand the role of vision and attentional focus, we added an additional visual stimuli to our external focus condition, as we wanted to maximize differences in brain activation congruent with manipulations that have demonstrated superior performance improvements with added visual stimuli.13 We hypothesized that (1) when participants completed the gross motor movement using an external focus of attention with additional visual stimuli, there would be more activation in areas of the brain associated with vision, specifically regions that integrate sensory information from the environment and (2) when participants completed the gross motor movement using an internal focus of attention without a visual stimuli, the data would reveal significantly more activation in areas of the brain associated with motor control, such as the motor cortex, as an internal focus is believed to elicit conscious control over motor movements.6–8
Methods
Participants
A total of 10 healthy, recreationally active participants (5 males, age 27 [6.2] y, height 177.0 [10.8] cm, mass 65.3 [7.9] kg; 5 females, age 30 [15] y, height 167.0 [10.8] cm, mass 62.7 [12.2] kg) were recruited from local universities. Inclusion criteria included no lower-extremity injury in the last 6 months and the left leg being the preferred stance limb when kicking a ball. Participants were excluded if they had (1) previous history of injury to the capsule, ligament, or menisci of either knee; (2) any vestibular or balance disorder; and (3) any metal or implanted medical device in the body that would be a contraindication to magnetic resonance imaging (MRI) assessment. All participants read and signed an informed consent form approved by the University of North Carolina at Greensboro Institutional Review Board for the protection of human subjects. Each participant attended a single testing session consisting of structural and functional neuroimaging via MRI.
Task and Procedure
Prior to scanning, participants received no direct instructions of how to complete the tasks. For functional imaging a block design was implemented in the scanner where participants completed 1 run each of an internal focus condition and external focus condition in random order. Using a variety of blocking pads and straps, great care was taken to minimize head motion. A brace was applied to the ankle joint to minimize ankle joint motion. A wedge was placed under the knee to allow the limb to move from approximately 45° flexion to terminal extension (±5° depending on femur length; Figure 1).19,20 Further, a mirror was attached to the head coil and positioned above the participants’ eyes to allow the participant full view of their feet and the surrounding environment. Each run consisted 4 sets of 30 seconds of rest followed by 30 seconds of approximately 45° unilateral knee extension–flexion movements triggered by an auditory metronome at 1.2 Hz with each run ending after 30 seconds of rest (4:30 scan time for each run). Each attentional focus condition was performed in a separate run to avoid attentional focus confusion on behalf of the participant and to minimize pollution of instruction between conditions. While positioned in the scanner participants were familiarized to the extension–flexion movements. Attentional focus instructions on how to complete the knee movements were given only immediately prior to the specified run and immediately prior to each of the 30-second contraction blocks. For the external focus condition, a small external target (5 cm × 5 cm white piece of tape attached to a string) was placed directly above the participant’s tibia. We elected to implement a visual target in our external focus manipulation as it has been demonstrated to further enhance performance relative to external focus instruction alone.13 Care was taken to ensure that the participant could see the target the entire time through the mirror, but could not touch the target with their limb. In this external focus condition participants were instructed: “please focus on extending toward the target while moving your limb to the metronome.” For the internal focus condition, participants were instructed: “please focus on squeezing your quadriceps while moving your limb to the metronome.” Participants’ field of view was constrained while in the scanner (ie, small window of vision), thus we deemed it appropriate to remove the target for the internal focus condition to isolate effects of internal focus instruction. The participant had the same field of view in both conditions, with the only difference being that there was no specific visual target during the rest and move blocks for the internal focus, whereas the visual target was present during all rest and move blocks for the external focus. We also acknowledge that asking participants to adhere to a metronome may have elicited a dual-task paradigm21,22; however, our contrast analyses allowed us to solely focus on instruction differences as the metronome sound and timing demands were present in both conditions.
—Participant moving their leg in the external focus condition while inside an magnetic resonance imaging scanner. The hanging target was removed during the internal focus condition.
Citation: Journal of Sport Rehabilitation 29, 4; 10.1123/jsr.2018-0026
fMRI Data Acquisition and Analysis
All scans were performed on a Siemens Magnetom Tim Trio 3.0 T MRI scanner using a 12-channel head coil (Siemens Medical Solutions; Erlangen, Germany). Following the methods of Grooms et al,19 T1-weighted structural images were initially obtained (repetition time = 2000 ms; echo time = 4.58 ms, matrix field of view =256 mm; voxel size = 1 mm × 1 mm × 1 mm). The fMRI imaging for each of the 3 runs included 93 whole-brain gradient-echo echoplanar scans (repetition time = 3000 ms; echo time = 28 ms, phase encoding direction = anterior to posterior; matrix field of view = 220 mm; voxel size = 2.5 mm × 2.5 mm × 2.5 mm). The first 3 volumes were discarded to account for scanner preparation and equilibration effects. This equated to 10 full-brain datasets per 30-second knee movement block, which resulted in 40 full-brain activation maps for knee movement (4 blocks) contrasted with 50 full-brain maps for rest (5 blocks) during each of the conditions.
The fMRI analyses were performed using the fMRI of the brain (FMRIB) software library (FSL: The Oxford Centre for Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom).23 Standard processing was completed. This included 4Dmean intensity normalization, temporal filtering (90 s), spatial smoothing at 6-mm full width at half maximum (FWHM), FMRIB’s improved linear model (FILM) prewhitening, interleaved slice timing correction, brain extraction, and fMRIB's linear image registration tool for motion correction (MCFLIRT).23–25 Next, data were denoised with the independent component analysis-based automatic removal of motion artifacts (ICA-AROMA) pipeline. ICA-AROMA decomposes the data and automatically identifies and removes components related to head motion.26 ICA-AROMA has been shown to be sensitive to motion artifacts while preserving task related data.27 While this investigation had minimal motion artifact due to extensive participant restraint by using ICA-AROMA, we further decreased the probability of head artifact-related activation being present between the contrasts. There was no statistical difference in absolute (external: 0.33 [0.18]; internal: 0.33 [0.18]; P = .93) or relative (external: 0.12 [0.07]; internal: 0.13 [0.07]; P = .45) head motion between conditions. Lower level subject contrast (knee movement − baseline [rest]) and higher level (external − internal focus conditions) were completed with a z threshold of 2.3 and P < .05 Gaussian random field cluster corrected.28–30 The higher level group analysis was completed with FMRIB’s local analysis of mixed effects stage 1 and stage 231 using 2 separate paired samples t tests to contrast the external focus and internal focus conditions (external focus > internal focus and internal focus > external focus).
Results
When contrasting the external focus to the internal focus during left unilateral knee extension, several right side regions demonstrated significantly greater activation. Full details of brain regions with significantly greater activation in the external focus condition relative to the internal focus condition are presented in Table 1 with visual representations displayed in Figure 2. When contrasting the internal focus to the external focus during left unilateral knee extension, several left side regions demonstrated significantly greater activation. Full statistical details of the brain regions with significantly greater activation in the internal focus condition relative to the external focus condition are presented in Table 2 with visual representations displayed in Figure 2.
External Focus > Internal Focus Contrast
| Montreal Neurological Institute coordinate of peak voxel | Z center of gravity | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Cluster index | Brain regions | Side | Voxels # | P value | x | y | z | Zmax | x | y | z |
| 1 | Occipital pole Cuneal cortex Lateral occipital cortex Intracalcarine cortex | Right | 1048 | <.001 | 12 | −94 | 18 | 6.22 | 13.9 | −86.4 | 22.7 |
| 2 | Lingual gyrus (anterior) Temporal occipital fusiform cortex Parahippocampal gyrus (posterior) | Right | 674 | <.001 | 32 | −46 | −4 | 4.46 | 32.2 | −41.6 | −12.7 |
| 3 | Lateral occipital cortex | Right | 337 | .01 | 46 | −80 | 6 | 3.95 | 46.4 | −78.9 | 5 |
Note: Brain regions with significant activation using a significance level set a priori at P < .05; Gaussian random field cluster corrected, and z threshold set at z > 2.3.
—Brain regions with increased activation (P < .001) during the external focus condition (colored orange and surrounded by solid circles) and internal focus condition (colored blue and surrendered by dashed circles). Note that the solid and dashed circles do not encompass the precise spatial characteristics of the activation clusters (to be used as a reference for black and white versions of the manuscript). (A) Posterior view, (B) anterior view, (C) left posterior–lateral view, and (D) right posterior–lateral view.
Citation: Journal of Sport Rehabilitation 29, 4; 10.1123/jsr.2018-0026
Internal Focus > External Focus Contrast
| MNI coordinate of peak voxel | Z center of gravity | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Cluster index | Brain regions | Side | Voxels # | P value | x | y | z | Zmax | x | y | z |
| 1 | Lingual gyrus Occipital pole Occipital fusiform gyrus | Left | 725 | <.001 | 2 | −80 | −6 | 4.28 | −10.1 | −82.1 | −4.58 |
| 2 | Lateral occipital cortex | Left | 473 | <.001 | −54 | −72 | 6 | 4.01 | −50.1 | −79.1 | −1.27 |
| 3 | Postcentral gyrus Heschl’s gyrus Precentral gyrus | Left | 301 | <.001 | −58 | −14 | 20 | 3.54 | 53.7 | −18 | 19.7 |
| 4 | Cerebellum: IX, VIIb | Left | 265 | .01 | −30 | −65 | −54 | 3.35 | −14 | −52.2 | −48 |
Note: Brain regions with significant activation using a significance level set a priori at P < .05; Gaussian random field cluster corrected, and z threshold set at z > 2.3.
Discussion
This study examined brain function differences during a gross motor movement using an internal and external focus of attention. A primary purpose was to identify brain regions involved when following instructions specific to an external focus of attention when directed toward a visual target during a gross motor movement. We were specifically interested in the regions that integrate the sensory information from the environment. A secondary goal was to determine if regions of the brain associated with motor control activate more when individuals follow internal focus instructions. The importance of this experiment is the use of fMRI to study the regions of the brain that activate during different instructional foci. Currently, the literature hypothesizes that an external focus promotes automaticity and an internal focus elicits conscious control over motor movement, therefore, this study assessed this role of each type of focus on brain activity measured using fMRI.
Congruent with our first hypothesis, an external focus of attention directed toward a visual target, relative to an internal focus of attention directed purely through instruction, increased activation in areas of brain regions associated with vision. Increased activation was detected in the occipital pole, cuneal cortex, anterior portion of the lingual gyrus, and intracalcarine cortex. The cuneal cortex, lingual gyrus, and intracalcarine cortex are located within the occipital pole which is highly responsive to visual stimuli32–34 and we believe that the added external target, relative to no visual target for internal focus, plausibly explains this increased activation. However, we did not include an external focus condition without a visual target to disentangle whether the increased visual region activation was a product of the external focus or the visual target. We also detected increased activation of the temporal-occipital fusiform gyrus cortex during the external focus condition directed toward a visual target. The occipital fusiform gyrus is highly involved with object recognition,35 which may suggest that an external focus augments sensory streaming, but requires further investigations that incorporate behavioral and sensory measures.36,37 Similarly, we found increased activation in the parahippocampal gyrus, which is associated with memory and encoding of environmental stimuli38 and complements the findings of Zentgraf et al16 that revealed increased somatosensory activation for an external focus.
Externally focused instructions can facilitate not only gross motor performance of a jumping task, but also kinematic values related to knee range of motion that could affect injury prevention.12 Following externally focused instructions, individuals increased peak knee flexion during a single-leg hop compared with the internally focused group.12 These differences can be explained by the constrained action hypothesis which states that when we pay attention (by using internal focus) to our movement output, we can disrupt the automaticity of a previously well-learned movement. Although the study is limited by lack of motor performance comparisons, our results provide information pertaining to the brain regions responsible for processing attentional focus instruction with and without additional visual stimuli within a controlled environment.
In support of our second hypothesis, we found that an internal focus increased activation in motor regions, specifically the precentral gyrus (ie, primary motor cortex or M1), the postcentral gyrus (ie, the supplementary motor cortex), and cerebellum. While participants performed the same motor task in both conditions under a controlled environment, the fMRI data revealed increased brain activity within motor regions when participants were given internal focus instruction. The primary role of the precentral gyrus is motor function, while integrating signals from the supplementary motor cortex to execute movement.39 Similarly, the supplementary motor cortex responsible for the planning and coordination of complex movements and is activated during real or imagined movements.40 The increased activation in motor regions for our internal focus condition is inconsistent with that of Zentgraf et al,16 but may due to the controlled nature of our task (as opposed to self-paced). Alternatively, it may be due to the gross motor task used in this study, but highlights the differences in brain activation that occur depending on skill type and instructional demands. In addition, we detected increased activation in Heschl’s gyrus during the internal focus condition. This region is located within the auditory cortex and contributes to auditory processing41 and tentatively supports the concept that individuals will experience increased cognitive demands when processing internal focus instruction. While the cerebellum has traditionally been considered to be primarily involved in motor function, it is increasingly understood to have a much wider function due to parietal and prefrontal lobe connections.42 Specifically Lobule VII of the cerebellum, which we demonstrate to be activated to a greater degree in the internal condition, has been associated with increased cognitive demands.43,44 This may indicate that an internal focus of attention may increase cognitive demand relative to external focus and warrants future investigations with complementary psychometric measures to assess attentional resources. During our internal focus manipulation, we also found increased visual region activation, specifically in the occipital fusiform gyrus and posterior region of the lingual gyrus. The occipital fusiform gyrus is involved with body recognition (eg, face recognition)45,46 and it is cautiously posited that internal focus instructions of “squeezing their quadriceps” engaged a similar neural recruitment strategy for limb recognition. However, it should be noted the blood oxygenation level dependent response captured here with fMRI is a secondary measure and has limitations and does not give complete insight into neural activity. It is possible other aspects of neurophysiology or individual cognitive states may contribute to the differences seen here.
Our choice of only including a visual target for our external focus condition may make it appear difficult to compare brain activation differences with the internal focus condition. While we are aware that standard attentional focus paradigms only manipulate instruction,3 this was intentional due to the logistics of our design. When inside an MRI scanner, the field of view displayed through the mirror is small relative to the standard field of view participants have when engaging in typical attentional focus paradigms (ie, participants can look in any direction). Pilot testing revealed that the placement of our target encapsulated nearly the entire field of view for participants. Therefore, if the target remained hanging for the internal focus condition, participants may have ignored our instruction and visually relied on the target for movement control. Thus, we contend that our data were a satisfactory initial step in understanding brain activity associated with attentional focus and gross motor control, but further research is warranted that manipulates the presence of additional visual stimuli. We also acknowledge that the use of the metronome was more in line with attentional focus manipulations that utilize dual-task methodology,2,17,47,48 but this was also intentional as attentional focus instruction can alter movement speed.49,50 We did not want to confound our neuroimaging data with the effects of attentional focus on movement speed.
Conclusions
The results from this study are the first to show brain activation differences during a gross motor task when following specific attentional focus instructions. Relative to internal focus direction, an external focus directed toward a visual target produced more cortical activity in brain regions associated with vision and ventral streaming pathways. This increased activation may increase the important, relevant, and goal-oriented aspects of the task, which could be influential in the development of positive neuroplasticity and provide a partial explanation for the beneficial effects of an external focus for motor learning. In contrast, relative to an external focus, internal focus increased activation in brain regions that are responsible for motor control. We believe that this is the first neural mechanistic data showing that an internal focus engages brain regions associated with motor control furthering our understanding of the deleterious effects of an internal focus. We consider that previous reports of poor neuromuscular efficiency,51 reduced maximal force production,11 and overall poorer performance resulting from an internal focus3 may be due to differences in cortical processing. Little attention has been given to positively affecting neurologic adaptations during orthopedic prevention and rehabilitation.52 Results from this study serve as baseline information for future prevention and rehabilitation investigations of how manipulating the focus of attention can constructively affect neural control during training and rehabilitation.
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