31
Journal of Vestibular Research 15 (2005) 31–39 IOS Press
Improved postural control through repetition and consolidation F. Tjernstr¨om∗ , P.-A. Fransson and M. Magnusson Department of Otorhinolaryngology, University Hospital of Lund, Lund, Sweden
Received 3 February 2004 Accepted 9 September 2004
Abstract. Research regarding the optimal frequency of training in postural control rehabilitation has been sparse. Posturography with vibratory proprioceptive stimulation was performed with eyes open and closed on 36 healthy subjects divided into 3 groups. Each group was tested 5 times, though with different time-intervals; 20 minutes, 3 hours and 24 hours respectively. Two different adaptive processes seems to be involved in the formation of a new movement pattern when exposed to a postural disturbance, one fast adaptation active during each test occasion and a second adaptation active between the consecutive tests. As the same adaptation pattern was found regardless the repetition time interval, the results imply either that the consolidation process of the new motor memory is time-independent or that the stimulus was sufficiently strong to induce fast consolidation thus leaving the time-interval unimportant. The findings suggest that it is primarily the number of repetitions in the exercises that governs the outcome of training, whereas the time interval between the exercises is of less importance. Keywords: Postural control, adaptation, consolidation, motor memory
1. Introduction Postural control is a complex feedback-dependent system using sensory input from the visual, vestibular and somatosensory receptors [14,28,45]. The sensory information provided are tested to each other and “reweighted” depending on what perception one relies most upon in any given situation [45]. The postural control system is considered to use an internal model of the body’s configuration and dynamics, which the central nervous system (CNS) utilize to restore the body’s balance [33] i.e. a high level process. The control system must continuously adapt and adjust to changing postural challenges, such as when the support surface changes from solid to slippery or if the support area is reduced [25], and in long perspective adapt and de∗ Corresponding
author: F. Tjernstr¨om, Department of Otorhinolaryngology, University Hospital of Lund, S-221 85 Lund, Sweden. Tel.: +46 46 171705; Fax: +46 46 2110968; E-mail: fredrik.
[email protected].
velop to the physiological changes through life from childhood to old age [5,7,11,31,44,48]. Improvements in posture control are dependent upon plasticity of neurons in different regions in the brain, and their interconnections and interactions [27,55]. The general paradigm is that new motor memory is formed from a short-term fragile state (on-line memory) through a time-dependent process known as consolidation [1,10,23,39,42,51]. On molecular level the consolidation process is thought to require protein synthesis and thus act within hours [8,10,13,37]. Some studies have shown an additional consolidation effect of sleep [19,35,46,52,57], but this is refuted by others [15]. The possibility of a consolidation process acting in a much shorter time-span, i.e. seconds [9,47] under certain circumstances, cast doubt over a simplistic standard consolidation procedure as a unified model for all types of learning. It could be that different motor memories are processed more quickly given the circumstances and that different neuromodulators in different situations act on the synapses plasticity [15].
ISSN 0957-4271/05/$17.00 2005 – IOS Press and the authors. All rights reserved
32
F. Tjernstr et al. / Improved postural control through repetition and consolidation
The medial temporal lobe (MTL) and the hippocampal complex is traditionally thought to be critical for memory development, primarily based upon brainlesion studies [1,4,24,34]. However, with the development of functional radiological imaging, new studies have shown that other regions seem to be involved in the consolidation process; primary motor cortex [27, 32,40,41,50], supplementary motor area [2], basal ganglia [22,49] and cerebellum [6,15,17,37,43]. Interestingly, the vestibular pathways has been shown to reach the hippocampus via thalamus, parietal cortex and the reticular formation [12,36,53], as well as it is connected to the cerebellum [53]. The significance of these interconnections in vestibular rehabilitation remains to be investigated. The ability to adapt to postural disturbances can be demonstrated by posturography [20,29]. Vibration applied to a muscle or a muscle tendon increases the firing of the muscle spindles, thus signaling that the muscle is being stretched. The stimulated muscle responds with a reflexive contraction (tonic vibratory reflex) [21]. In healthy subjects, body sway induced by repeated highintensity vibration usually decreases over time by adaptation [20]. Similar adaptive responses have been observed in healthy subjects during posturography using galvanic stimulation [29]. Both types of stimulation resulted in alterations of stance and the subjects became less sensitive to the disturbances during the stimulation period. We have previously described how normal subjects adapt and form long-term memory from repeated perturbations during vibratory posturography [54] and that motor memories, in accordance to Karni et al. [32], develop through at least two stages; a fast learning – within a training session and a slow learning – after continued practice. The objective with the present study is to determine whether the time interval between postural training sessions had any effect on the adaptation process and consolidation leading to formation of long-term memory.
had any recent (< 5 years) experience of similar tests. They were naive concerning the study protocol and the methods employed. None was using any medication except oral contraceptives. None had experienced any otoneurological, neurological, psychiatric, orthopedic or hearing disorder. Alcoholic beverages and sedative drugs were proscribed for 24 hours preceding the testing. Informed written consent was obtained from all the subjects and the experiments were done in accordance with the Helsinki Declaration of 1975. 2.2. Methods
2. Material and methods
Postural control was evaluated by perturbing stance while the test subjects stood on a force platform (400 × 400 × 75 mm) equipped with six strain-gauge sensors. Forces actuated by the feet were recorded with six degrees of freedom by a custom-made force platform developed at the Department of Solid Mechanics, Lund Institute of Technology. Data were sampled at 10 Hz by a computer equipped with a 12-bit AD converter. Perturbations mainly causing anteroposterior postural disturbances were induced by simultaneous vibratory stimulation to the belly of the gastrocnemius muscles of both legs [18]. The vibrations were applied to the muscles by two cylindrical vibrators (0.06 m long and 0.01 min diameter). The vibrators were held in place with an elastic strap around each leg. The vibration amplitude was 1.0 mm amplitude at a constant frequency of 85 Hz. Before the vibratory stimulation started, spontaneous sway was recorded for 30 seconds. The vibratory stimulation were executed according to a computer controlled pseudorandom binary sequence (PRBS) schedule [30] for 205 seconds by turning on/off the vibratory stimulation. Each test lasted 235 seconds including the quiet stance preceding the stimulation. The PRBS schedule was composed of stimulation shift periods (on) with random duration between 0.8– 6.4 seconds, which yielded an effective bandwidth of the test stimulus in the region of 0.1–2.5 Hz. Thus, the designated PRBS stimuli cover a broad power spectrum and the randomized stimulation reduces the opportunity to make anticipative and preemptive adjustments
2.1. Subjects
2.3. Procedure
The experiments were performed on 36 healthy paid volunteers (17 male, 19 female) aged 15–38 years (mean 25 years, SD 4 years), weight 41–100 kg (mean 67.5 kg, SD 13.1 kg), and with a body length of 160– 197 cm (mean 1.75 m, SD 0.09 m). None of the subjects
Posturography with vibratory proprioceptive stimulation was performed on 36 healthy subjects divided into 3 groups with 12 subjects each. The groups were tested 5 times, though with different intervals; 20 minutes, 3 hours and 24 hours respectively. A 6th follow-
F. Tjernstr et al. / Improved postural control through repetition and consolidation
33
Table 1 Statistical and amplitude comparisons between torque variance obtained between trial 1, trial 5 and trial 6 (3 months), during the quiet stance and stimulation period I–IV. The values from eyes closed tests are presented in table A and the values from eyes open tests are presented in table B. The trial comparisons that contained no significant variation are not shown in the tables A. Eyes closed Test period Quiet stance
Repetition time 20 minutes 3 hour 1 day
Trial 1/Trial 5 p-value Ampl. quotient ns 0.85 ns 1.68 ns 0.76
Trial 1/Trial 6 p-value∗ Ampl. quotient ns 1.08 ns 1.37 ns 0.77
Trial 5/Trial 6 p-value Ampl. quotient ns 1.27 0.041 0.81 ns 1.01
Period 1
20 minutes 3 hour 1 day
0.002 0.003 0.002
3.83 2.89 2.69
0.006 0.002 0.010
2.30 2.74 1.95
0.006 ns ns
0.60 0.95 0.73
Period 4
20 minutes 3 hour 1 day
0.002 0.003 0.005
2.74 2.19 2.15
0.023 0.005 ns
1.50 2.01 1.39
0.006 ns ns
0.55 0.92 0.64
B. Eyes open Test occasion uiet stance
Repetition time 20 minutes 3 hour 1 day
Trial 1/Trial 5 p-value Ampl. quotient ns 1.07 ns 1.70 ns 1.26
Trial 1/Trial 6 p-value∗ Ampl. quotient ns 2.32 ns 1.70 ns 1.35
Trial 5/Trial 6 p-value Ampl. quotient 0.011 2.17 ns 1.00 ns 1.08
Period 1
20 minutes 3 hour 1 day
0.002 0.003 0.004
4.13 3.29 3.07
0.023 0.002 0.004
2.61 2.25 2.29
ns ns ns
0.63 0.68 0.75
Period 4
20 minutes 3 hour 1 day
0.021 0.002 ns
2.00 2.35 1.46
0.019 0.034 ns
1.67 1.80 1.29
ns ns ns
0.84 0.77 0.88
*ns denote a not significant difference.
up trial was conducted after 3 months on all subjects. After brief information about the test procedure were the subjects equipped with vibrators on both calves’ rear aspects and placed on the force platform where headphones relaying music were attached. The subjects were instructed to stand erect but not at attention, with arms crossed over the chest and feet at an angle of about 30 degrees open to the front and the heals approximately 3 cm apart. Two tests were conducted at each trial occasion, one with the subjects’ eyes closed and the other with their eyes open and fixating on mark on the wall at a distance of 1.5 m. Half of the test subjects started each trial occasion with the eyes-open test, and the other half with the eyes-closed test. This order was maintained in the consecutive trials. 2.4. Data analysis The variance of anteroposterior body sway was obtained for five periods for each test: the quiet stance period (0–30 seconds) before stimulation, and from four periods (1–4) during the stimulation (30–80, 80–130, 130–180, and 180–230 seconds, respectively). Regression analysis of the torque variance showed dependence to the test subjects’ squared weight and height.
The torque variance data were therefore normalized by squared weight and squared height, and for representation purposes, multiplied by 1000. As vibratory stimulation applied to calf muscles mainly affects muscles predominantly active in the anteroposterior direction [18], only those responses were analyzed. The Wilcoxon non-parametric test [3] was used for the statistical comparison between the body sway during first, the fifth and the sixth (after 3 months) trials. The mean amplitude quotients shown in Table 1 are defined as [torque variance (period X, trial 1)/torque variance (period X, trial 5)]; [torque variance (period X, trial 1)/torque variance (period X, trial 6)] and [torque variance (period X, trial 5)/torque variance (period X, trial 6)], where period X is either the quiet stance period or stimulation period 1 to 4. Moreover, the Wilcoxon non-parametric test was also used for statistical comparison between the body sway during quiet stance compared to stimulation period 1, and the body sway in stimulation period 1 compared stimulation period 4 within each trial. The mean amplitude quotients shown in Table 2 are defined as [torque variance (period1)/torque variance (quiet stance)] and [torque variance (period4)/torque variance (period1)]. The MannWhitney test was used for statistical comparison between the body sway during test repeated with differ-
34
F. Tjernstr et al. / Improved postural control through repetition and consolidation
ent time intervals, i.e., 20 minutes, 3 hours and 1 day. Non-parametric statistics were used since the obtained values were not normally distributed after logarithmic transformation. In the analysis, a p-value < 0.05 was considered statistically significant except for the values presented in figure 1, where the significance level was lowered to p-value < 0.01, according to Bonferroni due to the multiple statistical analyses [3]. However, we still mark the found p-value < 0.05 in the figure for reasons of consistency. The adaptation during the five initial trials and during the consecutive test periods throughout stimulation, stimulation periods 1–4, was analyzed with linear and exponential regression to evaluate the relative dependency of repetition of the tests and dependency of the time period during the stimulation.
3. Results
3.2. Adaptation during the consecutive test periods The anteroposterior body sway was considerably increased by vibratory stimulation during most trials with eyes closed and most prominently during the first and sixth trial with eyes open (Table 2). It is noteworthy that the quotient values were proportionally higher with 3 hours repetition interval during the fifth trial both during the tests with eyes closed and eyes open. Noteworthy is also the proportionally lower quotient values with 1 day repetition interval during the sixth trial (3 month control) both during tests with eyes closed and eyes open (Table 2). Most variance values were substantially reduced during the first trial from stimulation period 1 to period 4 mainly during tests with eyes closed (p < 0.05). However, the body sway reduction during the test progress was much weaker during the fifth and sixth trials especially during tests with eyes open.
3.1. Adaptation between consecutive test occasions
3.3. Adaptation between consecutive tests occasions and during consecutive test periods
Figure 1 shows the anteroposterior torque variance values during the consecutive test occasions during quiet stance, stimulation period 1 and stimulation period 4. There was clear sway deterioration both during the tests and between the consecutive test occasions during the stimulation period. However, the body sway during quiet stance was not apparently changed by the repeated tests. Interestingly, the time interval between the repeated trials had no significant influence on the body sway during the trials. The statistical comparisons were at three occasions below p < 0.05 but not below 0.01. The significant difference found by the statistical comparison between values obtained trial 1, 5 and 6 are presented in Table 1. There was a prominent reduction of the torque variance to the vibratory stimulation both during eyes closed and eyes open tests from trial 1 to trial 5. The torque variance was somewhat increased between trial 5 and trial 6 (3 months) but the values did not increase to the same level as that of trial 1, demonstrating a retained skill. The time interval between the repeated trials had no major influence on the body sway during the trials, even if the body sway reduction was somewhat lower with eyes open during period 4 when the trials were repeated with 1-day interval.
Table 3 shows the results from the linear and exponential regression analysis between torque variance data and the Consecutive Trials and Consecutive Test Periods parameters. The Consecutive Trials regression parameter expresses the body sway dependency on adaptation between the consecutive trials. There was an apparent dependency both during eyes closed and eyes open tests to the trial parameter. The p-values acquired by linear or exponential regression were almost identical so it was not feasible to determine whether the sway reductions obtained by daily repeating the tests was linear or exponential reduced. The Consecutive Test Periods regression parameters express the body sway dependency on the test period 1–4 during the stimulation, e.g., adaptation during the same trial. The reduction of the torque variance values was somewhat more linear dependent to the test period regression parameter and the body sway reduction was most prominent during tests with eyes closed. The regression analysis suggests that the body sway reduction during consecutive trials and consecutive test periods within the trial is not substantially different whether the trials is repeated with 20 minutes, 3 hours or 1 day time intervals.
F. Tjernstr et al. / Improved postural control through repetition and consolidation
35
Table 2 Statistical and amplitude comparisons between the anteroposterior torque variance during quiet stance compared to stimulation period 1, and the body sway in stimulation period 1 compared period 4 for trials repeated with respectively 20 minutes, 3 hours and 1 days time interval A. eyes closed Test occasion Trial 1
Repetition time 20 minutes 3 hour 1 day
Period 1-quiet stance p-value Ampl. quotient 0.002 11.27 0.002 8.09 0.002 9.04
Period 4-Period 1 p-value∗ Ampl. quotient 0.003 0.46 0.002 0.45 0.004 0.52
Trial 5
20 minutes 3 hour 1 day
0.005 0.002 0.004
2.51 4.71 2.56
0.010 0.019 ns
0.64 0.59 0.65
Trial 6
20 minutes 3 hour 1 day
0.002 0.002 0.003
5.29 4.04 3.55
ns 0.003 ns
0.70 0.61 0.73
B. eyes open Test occasion Trial 1
Repetition time 20 minutes 3 hour 1 day
Period 1-Quiet stance p-value∗ Ampl. quotient 0.002 5.60 0.002 5.27 0.028 3.31
Period 4-Period 1 p-value∗ Ampl. quotient 0.028 0.51 ns 0.54 ns 0.52
Trial 5
20 minutes 3 hour 1 day
ns 0.002 ns
1.45 2.72 1.35
ns ns ns
1.05 0.76 1.09
Trial 6
20 minutes 3 hour 1 day
0.002 0.005 ns
4.98 3.99 1.95
ns ns ns
0.79 0.67 0.93
*ns denote a non-significant difference.
4. Discussion The findings suggest that adaptation to a novel postural challenge cause the generation of a modified motion strategy, reflected by both quantitatively and qualitatively alterations of the body sway responses. This process of adaptation could be defined as “consolidation”, as the postural strategy during inactivity has been refined and the motor responses further improved [24,50]. Moreover, the results imply either that the consolidation process of the new improved motor output appears to be time-independent, or that the vibratory stimulus used is sufficiently strong to induce fast consolidation [47]. Another explanation could be that the adaptation of the postural control system is complex and integrates sensory input as well as motor output. “Sensory training” act on a shorter time-scale than “motor training” [32] and vibratory posturography measure a sensorimotor system, thus there might be a completely different time constant in this kind of consolidation processes. The main conclusion from this study is that it is primarily the number of repetitions in an exercise that governs the outcome of training, whereas the time interval between the exercises is of less importance. However, the results in Table 1; regarding the significant increase of sway in the 20 minute group when retested after 3
months, and in Table 2; the lack of significant decrease of sway in the 1 day group during last period trial 5 and 6, could argue for a finer tuning of the postural responses, i.e. a more effective consolidation when the interval was 1 day between the tests. This study shows that at least two different adaptive processes seem to be involved in the formation of a new movement pattern when exposed to a postural disturbance. This is in line with our previous results [54] as well as with Karni et. al. [32]. The first adaptive process was observed as a sway reduction within the test progress and the adaptive process comprised both of linear and exponential components (Table 3: Consecutive test periods). In this way the postural control system change the motor strategy either to counteract the effect of the postural disturbance, or reduce the effect of the erroneous receptor information. Such changes in the motion responses were observed in the rapidly reduced body sway mainly during the initial 100–120 seconds of stimulation, which contained 20–30 perturbations. This number of perturbations appears to be sufficient to instigate a new or modified control strategy (internal model) in this study and in similar posturographic setups [20,29]. A fast adaptational behavior might be essential for an organism to survive a changing environment [16]. To wait for feedback-relayed mechanisms to fully develop may
36
F. Tjernstr et al. / Improved postural control through repetition and consolidation
A. Quiet Stance 4.0
3.0
Eyes Closed
Eyes Open
20 minutes
Torque Variance
3 hours
3.0
1 day
2.0
*
2.0 1.0
*
1.0
0.0
0.0 Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
B. Stimulation period 1
Torque Variance
30
12
Eyes Closed
Eyes Open
20 minutes 3 hours
10
1 day
20
8 6
10
4 2 0
0 Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
C. Stimulation period 4
Torque Variance
12
6.0
Eyes Closed
Eyes Open
20 minutes 3 hours
10
1 day
4.0
8 6
* 2.0
4 2 0
0.0 Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
Trial 1
Trial 2
Trial 3
Trial 4
Trial 5
3 Months
Fig. 1. Box-wisker plot of the normalized torque variance [Nm/(Kg*m)]2 during the six trial occasions and for three repetition time intervals. The box represents the interquartile range and the line across the box indicates the median. The “whiskers” are lines that extend from the box to the highest and lowest values, excluding outliers. No outliers and extreme values are displayed in the figures. The results are presented for eyes closed and eyes open tests during (A) Quiet stance (0–30 s); (B) stimulation period 1 (30–80 s) and (C) stimulation period 4 (180–230 s). Note the sway deterioration both during the tests and between the consecutive test occasions. (∗ = p < 0.05).
take too long time. Instead the CNS may use a program or an internal model that adapt to the new situation, in a manner of a “feed-forward control”, i.e. CNS simulates the dynamic behavior by predicting its next stage [58]. The reduction of the body sway followed mostly a linear behavior and the sway reduction was more prominent during tests with eyes closed.
A second, more long-term adaptive process or habituation was shown by the improvements gained by the daily repetition of the tests (Table 3: Consecutive trials and Fig. 1). At the start of each day, the response to the perturbations was controlled more efficiently than on the previous day. Based on previous experience, subjects were able to further refine the strategy and re-
F. Tjernstr et al. / Improved postural control through repetition and consolidation
37
Table 3 Statistical dependencies (p-values) in the torque variance found to repeated test occasions and to consecutive test period with a trial using linear (A) and logarithmic (B) regression A. Linear regression Repetition time Test 20 minutes Eyes closed Eyes open
Consecutive trials p-value Slope coefficient (b)1 < 0.001 −1.00 (0.20) 0.001 −0.38 (0.09)
Consecutive test periods p-value∗ Slope coefficient (b)1 0.037 −0.57 (0.25) ns −0.13 (0.12)
3 hour
Eyes closed Eyes open
< 0.001 < 0.001
− 0.92 (0.19) − 0.28 (0.06)
0.037 ns
−0.54 (0.24) − 0.12 (0.07)
1 day
Eyes closed Eyes pen
< 0.001 0.001
− 0.61 (0.11) − 0.29 (0.07)
0.020 0.048
− 0.34 (0.13) − 0.19 (0.09)
B. Exponential regression Repetition time Test 20 minutes Eyes closed Eyes open
Consecutive trials p-value Slope coefficient (b)1 < 0.001 − 0.24 (0.03) < 0.001 − 0.19 (0.03)
Consecutive test periods p-value∗ Slope coefficient (b)1 0.014 − 0.12 (0.04) ns − 0.03 (0.04)
3 hour
Eyes closed Eyes open
< 0.001 < 0.001
− 0.24 (0.04) − 0.22 (0.03)
0.036 ns
− 0.12 (0.05) − 0.06 (0.04)
1 day
Eyes closed Eyes pen
< 0.001 < 0.001
− 0.20 (0.03) − 0.18 (0.04)
0.013 ns
− 0.10 (0.03) − 0.09 (0.05)
1 Estimated
slope coefficient and standard deviation (SD) for the respective time range used (i.e., 20 minutes, 3 hours or 1 day for Trial occasions variable and 50s stimulation period for the Period variable). *ns denote a not significant difference.
duce the energy expended on correctional movements to withstand the perturbations. The linear and exponential regression gave almost identical result so it was inconclusive whether there was a linear or exponential dependent reduction of induced sway by daily repetitions. The above observations indicate that an adaptation to a novel postural challenge generates a motion strategy that both quantitavely and qualitatively affects the body sway responses. This strategy was further refined and contained, demonstrated by the test after 3 months (Table 1 and Fig. 1), which constitute a long-term motor memory [10]. The study further indicates that postural control needs to be sufficiently challenged by the stimulation or postural disturbance to induce adaptation by active learning. No adaptation to the stimulation were detected in similar studies when a vibratory stimulation with fewer perturbations and of lower amplitude was used [26,56], although the exercises were repeated at several occasions. This is in line with our observations that the body sway was unchanged during the rest periods over the consecutive test days. However, if stance was perturbed by larger disturbances, the experience from previous parts of the test and experience from repeated test occasions gradually reduced the body sway induced by perturbations [20,29].
5. Conclusion It is primarily the number of exercises performed that governs the outcome of postural rehabilitation, whereas the time interval between the exercises appears to be of less importance. Two different adaptive processes in postural control can be recognized; one immediate within the session and a second consolidation of the improved sensorimotor system. References [1]
[2]
[3] [4]
[5]
[6]
[7]
T. Abel and K.M. Lattal, Molecular mechanisms of memory acqusition, consolidation and retrieval, Current Opinion in Neurobiology 11 (2001), 180–187. H. Aizawa, M. Inase, H. Mushiake, K. Shima and J. Tanji, Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery, Exp. Brain Res. 84 (1991), 668–671. D. Altman, Practical statistics for medical research, New York: Chapman&Hall, 1991. P. Alvarez and L.S. Squire, Memory consolidation and the medial temporal lobe: a simple network model, Proc. Natl. Acad. Sci. USA 91 (1994), 7041–7045. C. Assaiante, Development of locomotor balance control in healthy children, Neurosci Biobehav Rev. 22(4) (1998), 527– 532. P.J.E. Attwell, S.F. Cooke and C.H. Yeo, Cerebellar function in consolidation of a motor memory, Neuron 13, 34(6) (2002), 1011–1020. R. Baloh, T. Fife, L. Zwerling, T. Socotch, K. Jacobson, T. Bell and K. Beykirch, Comparison of static and dynamic posturography in young and older normal people, J Am Geriatr Soc. 42(4) (1994), 405–412.
38 [8]
[9]
[10] [11]
[12]
[13]
[14]
[15]
[16]
[17]
[18] [19]
[20]
[21]
[22]
[23]
[24] [25]
[26]
[27] [28]
F. Tjernstr et al. / Improved postural control through repetition and consolidation M. Baudry, Synaptic plasticity and learning and memory: 15 years of progress, Neurobiology of learning and memory 70 (1998), 113–118. V. Bohbot, P. Ot´ahal, Z. Liu, L. Nadel and J. Bures, Electroconvulsive shock and lidocaine reveal rapid consolidation of spatial working memory in the water maze, Proc. Natl. Acad. Sci. USA 93 (1996), 4016–4019. T. Brashers-Krug, R. Shadhmehr and E. Bizzi, Consolidation in human motor memory, Nature 382 (1996), 252–254. Y. Breniere and B. Bril, Development of postural control of gravity forces in children during the first 5 years of walking, Exp Brain Res 121(3) (1998), 255–262. P.C. Cuthbert, D.P. Gilchrist, S.L. Hicks, H.G. MacDougall and I.S. Curthoys, Electrophysiological evidence for vestibular activation of the guinea pig hippocampus, NeuroReport 11(7) (2000), 1443–1447. J. DeZazzo and J. Tully, Dissection of memory formation: from behavioral pharmacology to molecular genetics, Trends Neurosci 18 (1995), 212–218. H. Diener and J. Dichgans, On the role of vestibular, visual and somatosensory information for dynamic postural control in humans, presented at Progress in Brain Research, Amsterdam, 1988. O. Donchin, L. Sawaki, G. Madupu, L.G. Cohen and R. Shadhmehr, Mechanisms influencing acquistion and recall of motor memories, J. Neurophysiol. 88 (2002), 2114–2123. M.C. Dorris, M. Par´e and D.P. Munoz, Immediate neural plasticity shapes motor performance, J. Neurosci. 20 (2000), RC52:1–5. J. Doyon, A.W. Song, A. Karni, F. Lalonde, M.M. Adams and L.G. Ungerleider, experience-dependent changes in cerebellar contributions to motor sequence learning, Proc. Natl. Acad. Sci. USA 99 (2002), 1017–1022. G. Eklund, Further studies of vibration-induced effects on balance, Upsala J Med Sci 78 (1973), 65–72. S. Fischer, M. Hallschmid, A.L. Elsner and J. Born, Sleep forms memory for finger skills, Proc. Natl. Acad. Sci. USA 99 (2002), 11987–11991. P.A. Fransson, R. Johansson, A. Hafstr¨om and M. Magnusson, Methods for evaluation of postural control adaptation, Gait Posture 12(1) (2000), 14–24. G. Goodwin, D. McCloskey and P. Matthews, Proprioceptive illusion induced by muscle vibration-Contribution by muscle spindles to perception, Science 175 (1972), 1382–1384. A.M. Graybiel, Building action repertoires: memory and learning functions of the basal ganglia, Curr. Opin. Neurobiol. 5 (1995), 733–741. E. Guigon and Y. Burnod, Short-term memory, in: The handbook of brain theory and neural networks, M.A. Arbib, ed., Cambridge, UK: The MIT Press, 1998, pp. 867–871. M.E. Hasselmo and J.L. McClelland, Neural models of memory, Curr. Opin. Neurobiol. 9 (1999), 184–188. F.B. Horak and L.M. Nashner, Central programming of postural movements: Adaptation to altered support-surface configurations, J Neurophysiol 55 (1986), 1369–1381. H. Ishizaki, I. Pyykk¨o, H. Aalto and J. Starck, Repeatability and effect of instruction of body sway, Acta Otolaryngol Suppl (Stockh) 481 (1991), 589–592. A. Jackson and R.N. Lemon, Motor control: Forcing neurons to change, Current Biology 11 (2001), R708–R709. R. Johansson and M. Magnusson, Human postural dynamics, CRC Crit Rev Biomed Eng 18 (1991), 413–437.
[29]
[30] [31]
[32]
[33]
[34]
[35]
[36]
[37]
[38] [39] [40]
[41]
[42] [43]
[44]
[45] [46]
[47] [48]
R. Johansson, M. Magnusson and P.A. Fransson, Galvanic vestibular stimulation for analysis of postural adaptation and stability, IEEE Trans Biomed Eng 42 (1995), 282–292. R. Johansson, System Modeling and Identification. Englewood Cliffs, NJ: Prentice Hall, 1993. J. Judge, M. King, R. Whipple, J. Clive and L. Wolfson, Dynamic balance in older persons: effects of reduced visual and proprioceptive input, J Gerontol A Biol Sci Med Sci 50(5) (1995), M263–M270. A. Karni, G. Meyer, C. Rey-Hipolito, P Jezzard, M. Adams, R. Turner and L. Ungerleider, The acquisition of skilled motor perfomance: Fast and slow experience-driven changes in primary motor ortex, Proc Natl Acad Sci USA 95 (1998), 861– 868. A. Kavounoudias, J.-C. Gilhodes, R. Roll and J.-P. Roll, From balance regulation to body orientation: two goals for muscle proprioceptive information processing, Exp Brain Res 124 (1999), 80–88. B.J. Knowlton and M.J. Fanselow, The hippocampus, consolidation and on-line memory, Curr. Opin. Neurobiol. 8 (1998), 293–296. H.S. Kudrimoti, C.A. Barnes and B.L. McNaughton, Reactivation of hippocampal cell assemblies: effect of behavioral state, experience and EEG dynamics, J. Neuroscience 19(10) (1999), 4090–4101. I. Pyykk¨o and M. Magnusson, Neural activity, alertness and visual orientation in intact and unilaterally labyrinthectomized rabbits, ORL J. Otorhinolaryngol. Relat. Spec. 49(1) (1987), 26–34. D.A. McCormick, G.A. Clark, D.G. Lavond and R.F. Thompson, Initial localization of the memory trace for a basic form of learning, Proc. Natl. Acad. Sci. USA 79 (1982), 2731–2735. J.L. McGaugh, Memory – a century of consolidation, Science 287 (2000), 248–251. J.L. McGaugh, Time-dependent processes in memory storage, Science 153 (1966), 1351–1358. D. McKay, R. Brooker, P. Giacomin, M. Ridding and T. Miles, Time course of induction of increased human motor cortex excitability by nerve stimulation, NeuroReport 13(10) (2002), 1271–1273. W. Muellbacher, U. Ziemann, J. Wissel, N. Dang, M. Kofler, S. Facchini, B. Boroojerdi, W. Poewe and M. Hallett, Early consolidation in human primary motor cortex, Nature 415 (2002), 640–644. Nadel, Bohbot Consolidation of memory, Hippocampus 11 (2001), 56–60. R. Nezafat, R. Shadhmehr and H.H. Holcomb, Long-term adaptation to dynamics of reaching movements: a PET study, Exp. Brain Res. 140 (2001), 66–76. P. Perrin, C. Jeandel, C. Perrin and M. Bene, Influence of visual control, conduction, and central integration on static and dynamic balance in healthy older adults, Gerontology 43(4) (1997), 223–231. R.J. Peterka Sensorimotor integration in humanpostural control, J. Neurophysiol 88 (2002), 1097–1118. W. Plihal and J. Born, Memory consolidation in human sleep depends on inhibition of glucocorticoid release, NeuroReport 10 (1999), 2741–2747. I.Y. Podolski, Possibility of superfast consolidation of long– term memory, Membr. Cell Biol. 11 (1998), 743–752. T. Prieto, J. Myklebust, R. Hoffmann, E. Lovett and B. Myklebust, Measures of postural steadiness: differences between healthy young and elderly adults, IEEE Trans Biomed Eng 43(9) (1996), 956–966.
F. Tjernstr et al. / Improved postural control through repetition and consolidation [49] [50] [51]
[52]
[53] [54]
D.P. Salmon and N. Butters, Neurobiology of skill and habit learning, Curr. Opin. Neurobiol. 5 (1995), 184–190. R. Shadhmehr and H. Holcomb, Neural correlates of motor memory consolidation, Science 277 (1997), 821–825. R. Shadmehr and Brashers-Krug, Functional stages in the formation of human long-term motor memory, J Neurosci 17(1) (1997), 409–419. B. Shen and B.L. McNaughton, Modeling the spontaneous reactivation of experience-specific hippocampal cell assembles during sleep, Hippocampus 6 (1996), 685–692. P.F. Smith, Vestibular-hippocampal interactions, Hippocampus 7 (1997), 465–471. F. Tjernstr¨om, P.-A. Fransson, A. Hafstr¨om and M. Magnusson, Adaptation of postural control to perturbations – a pro-
[55]
[56]
[57]
[58]
39
cess that initiates long-term motor memory, Gait and Posture 15 (2002), 75–82. E. Tulving and H.J. Markowitsch, Memory beyond the hippocampus, Current Opinion in Neurobiology 7 (1997), 209– 216. S. Uimonen, K. Laitakari, R. Bloigu and M. Sorri, The repeatability of posturographic measurements and the effects of sleep deprivation, J Vest Res 4(1) (1994), 29–36. M.A. Wilson and B.L. McNaughton, Reactivation of hippocampal ensemble memories during sleep, Science 265 (1994), 676–679. D.M. Wolpert, Z. Ghahramani and M.I. Jordan, An internal model for sensorimotor integration, Science 269 (1995), 1880– 1882.
