www.elsevier.com/locate/cogbrainres

Cognitive Brain Research 20 (2004) 92–97

Research report

Decay of prism aftereffects under passive and active conditions

Juan Fernandez-Ruiza,b,*, Rosalinda Dıaza, Carlos Aguilara, Cynthia Hall-Haroa

aDepartamento de Fisiologıa, Facultad de Medicina, Universidad Nacional Autonoma de Mexico, Ciudad Universitaria CP 04510,

Mexico City, D.F., Apartado Postal 70-250, MexicobEscuela de Psicologıa, Universidad Anahuac, Mexico

Accepted 22 January 2004

Available online 5 March 2004

Abstract

In prism adaptation, subjects adapt to new visuospatial coordinates imposed by wedge prisms that laterally displace the visual field.

During this process, subjects develop and store new visuomotor coordinates in order to compensate for the displacement of visual stimuli.

After the prisms are removed, subjects show an aftereffect in the opposite direction of the original perturbation. The aftereffect is a

manifestation of the recently stored information. In the present article, we were interested in studying the properties of the aftereffect.

Specifically, we investigated the fate of the aftereffect under active conditions with motor reafferences but without visual input, and during

passive conditions without visual or motor reafferences. The results in the motor active condition show that motor reafference (proprioceptive

or corollary discharge information) led to a faster, but incomplete, aftereffect decay. The results in the passive condition show a bimodal

aftereffect behavior, with a fast decay within the initial minutes, followed by a sustained aftereffect up to 20 min later. These data suggests

that two different memory processes may contribute to the aftereffect, one showing a fast decay mainly within 1 min, and another that shows

a stable endurance for more than 20 min.

D 2004 Elsevier B.V. All rights reserved.

Theme: Neural basis of behavior

Topic: Learning and memory

Keywords: Prism adaptation; Memory consolidation; Memory endurance; Memory decay; Visuomotor learning

1. Introduction in the form of skilled behavioral and cognitive procedures

When wedge prisms are donned, the induced visual

perturbation produces an alteration of the normal visuomo-

tor relationship. Prism adaptation refers to the modification

of that relationship in order to acquaint for the perturbation

induced by the prisms. The withdrawal of the prism during

that process produces an aftereffect in the opposite direction

of the original perturbation, proportional to the adaptation

magnitude acquired before removing the prisms [4].

The whole prism adaptation process has been proposed

to be a form of procedural learning (4), since it conforms

nicely to Tulving’s definition of a procedural memory

system as an action system whose operations are expressed

0926-6410/$ - see front matter D 2004 Elsevier B.V. All rights reserved.

doi:10.1016/j.cogbrainres.2004.01.007

* Corresponding author. Tel.: +52-55-56232123; fax: +52-55-

56363695.

E-mail address: jfr@servidor.unam.mx (J. Fernandez-Ruiz).

independent of any cognition [18]. It also falls within the

boundaries of Squire’s nondeclarative learning definition

that states that this kind of learning takes place when

experience accumulates in behavioral change without

affording conscious access to any memory content [16].

Viewed from this perspective, prism adaptation offers an

important advantage for studying visuomotor learning, a

specific kind of procedural learning, because it can dissoci-

ate performance from learning and memory. In a typical

experiment, the behavioral modification elicited by the use

of the prisms provides a learning estimate. Upon removal of

the prisms, the aftereffect provides a measure of the persis-

tence of the memory.

Although there have been large efforts in order to

understand prism adaptation [8,14,20], little is known

about the fate of the new visuomotor map formed during

this process. An important question that remains unre-

J. Fernandez-Ruiz et al. / Cognitive Brain Research 20 (2004) 92–97 93

solved is if the new visuomotor mapping formed during

prism adaptation decays spontaneously in passive condi-

tions or remains unchanged ready to be used in the next

visuomotor interaction. Previous reports addressing this

issue have tested the same subjects at different time

intervals after doffing the prisms [2,3,7,11–13,17]. How-

ever, those studies did not tested the aftereffect decay

under passive conditions because subjects still received

proprioceptive or motor feedback (corollary discharge)

information derived from the motor activity during each

testing [1]. This pose two problems: first, after the initial

aftereffect trial, the subsequent trials can be contaminated

by cognitive factors because the subjects realise that they

err even without prisms [19]; and second, and most

important, since the adaptation–readaptation process is

dependent on the number of visuomotor interactions [4],

the observed decay at different intervals could have been

the result of the accumulated interactions used to test

previous delays (i.e. the test at 15 min was preceded by

the tests at 5 or 10 min). It has been demonstrated in

prism adaptation experiments that muscular proprioceptive

information plays a role in the acquisition and retrieval of

motor memory. For example faster aftereffect extinctions

are found if muscular load or velocity are matched

between the adaptation and aftereffect phases [5,6]. How-

ever, it is not currently known if motor reafferences,

without visual reafferences, are capable of affecting the

extinction of the new visuomotor mapping [1]. For this

reason in the present study, we tested the influence of

motor activity, similar to the one used during prism

adaptation, on the decay function of the aftereffect. The

results obtained suggested that even without visual feed-

back, the more motor activity, the faster the aftereffect

decay. These results granted testing the passive decay

function at different time intervals but using independent

groups. The results obtained from the passive decay, without

any kind of reafference, suggested the possibility to divide

the aftereffect decay in two phases: one, lasting only a

couple of minutes that shows a fast 40% decay, and a second

phase, showing no decay at all, lasting at least 20 min.

2. Experiment 1

Since it is possible that motor reafferent stimulation has a

role in the aftereffect decay, the first experiment was

designed to test if execution of movements similar to those

used during the acquisition, but without visual feedback,

had some effect on the aftereffect extinction.

2.1. Materials and methods

2.1.1. Subjects

Forty right-handed healthy subjects between the ages of

18 and 24 participated as volunteers in this experiment. Half

of the subjects were female and the other half was male. The

subjects were naive to the purpose of the experiment and

gave informed consent to participate prior to the experi-

ments in accordance with the Declaration of Helsinki.

2.1.2. Basic prism adaptation paradigm

We followed the prism adaptation throwing technique

previously described [4]. Subjects threw clay balls (weight:

10 g) to a 12� 12 cm cross drawn on a large sheet of parcel

paper centered at shoulder level and placed 2 m away from

them. The subjects were instructed to make each toss

overhand during the whole experiment, and were asked to

throw the balls to the location where they saw the target.

The subjects performed the task from a standing position

and had an unobstructed view of the target during the entire

session. The head was unrestrained, and no directions were

given about trunk, shoulder, or head/neck posture. However,

they were not allowed to look down at their hand as they

collected the next ball from a tray located right next to their

bodies. A baseline throwing motor performance was

obtained by having the subjects throw 26 balls at the target

previous to the donning of the prisms (condition PRE). The

position at which the balls made an impact on or around the

target was marked immediately after each throw. After

donning 30-diopter prisms, the subjects were instructed to

throw 26 more balls in the same way (condition PRI;

adaptation phase).

2.1.3. POS manipulation

Before beginning the experiment, subjects were divided

into two groups of 20 subjects each. Both groups followed

the same PRE and PRI conditions previously described.

After finishing their last PRI throw, they were asked to close

their eyes before the post-prism testing (POS condition)

began. During the POS conditions, after doffing the prisms,

the first group was asked to remain with their eyes closed

while making 13 throws to where they had seen the target

previously, before opening their eyes to continue making 13

more throws to the, now visible, target. The second group

followed the same instructions but instead of doing 13

throws, they made 26 throws with their eyes closed before

they continue making 13 more throws to the visible target.

During the throws made with the closed eyes, the subjects

were asked to remain stood without making major body

movements, just as they were while making the PRI throws

that preceded the POS phase.

Three measures were calculated from the collected data.

First, an adaptation measure was obtained by subtracting the

distance to the center of the ball’s impact on the final throw

while wearing the prisms, from that on the initial throw

while wearing them. Second, a POS with eyes closed

condition was the measurement of the ball’s impact to the

target on the first throw with the eyes closed after removing

the prisms. And the third measurement was the aftereffect

that was defined as the ball’s impact horizontal distance to

the target on the first throw with the eyes open after testing

with the eyes closed.

tive Brain Research 20 (2004) 92–97

2.1.4. Statistical analysis

Student’s t-tests were used to compare independent

groups. To compare data within groups, paired t-tests were

used.

2.2. Results and discussion

The raw data obtained in this experiment is shown in

Fig. 1A and B. The horizontal mean distance from the

target in the POS condition with the eyes closed suggest

that subjects in both groups were capable of centering

their throws around the target, even though they were not

looking at it (x = 0. 68 +� 0.73 and 0.15 +� 0.53). A

Student’s t-test showed that there were no differences

between both groups (t = 0.576, DF = 37; p = 0.56 ns).

J. Fernandez-Ruiz et al. / Cogni94

Fig. 1. Raw data obtained in conditions PRE, PRI and POS for the 13

throws group (A) and the 26 throws group (B). Circles depict throws made

with the eyes open, and rhombus depict throws made with the eyes closed;

arrows indicate the first POS throw with the eyes open; (C) shows the POS

(aftereffect) data in absolute values for the first throw with the eyes closed

(black bars) and the first throw with the eyes open (gray bars) for both

groups. *Denotes significant difference at p< 0.05. Error bars = S.E.M.

However, the most relevant results are those concerning

the aftereffect, once the subjects were instructed to open

their eyes again. A paired t-test comparison of the last

PRE baseline throw vs. the first POS throw with eyes

open showed significant differences in both groups, sug-

gesting a preservation of the acquired visuomotor map

(t = 6.39, DF = 19; p < 0.001 for the 13 throws group;

t = 4.86, DF = 19; p< 0.01 for the 26 throws group). Fig.

1C shows the first throw with the eyes closed and the first

throw with the eyes open during POS for both groups. A

comparison of the first throw with eyes open in the POS

condition between both groups revealed a significant decay

of the 26 throws vs. the 13 throws group (t =� 2.22,

DF = 38; p = 0.03). These results suggest that even though

the motor reafference by itself does not completely abolish

the aftereffect it does produce a faster decay.

3. Experiment 2

The first experiment suggests that motor activity, similar

to the one used when adapting, lead to faster aftereffect

extinction. Since previous studies of the aftereffect decay

function tested the same subjects at different intervals, it

could be possible that their results were contaminated by

the subjects’ activity during testing. In this experiment, we

studied the aftereffect decay function in independent

groups under passive conditions without visual or motor

reafferences.

3.1. Materials and methods

3.1.1. Subjects

One hundred right-handed healthy subjects between the

ages of 18 and 24 participated as volunteers in this study.

Half of the subjects were female and the other half was

male. The subjects were naive to the purpose of the

experiment and gave informed consent to participate prior

to the experiments in accordance with the Declaration of

Helsinki.

3.1.2. Basic prism adaptation paradigm

We followed the same basic paradigm, except that after

removing the prisms used in the PRI condition, the subjects

threw 26 more balls to the target with the eyes open

(condition POS).

Three measures were calculated from the collected data.

First, an adaptation measure was obtained by subtracting the

distance to the center of the ball’s impact on the final throw

while wearing the prisms, from that on the initial throw

while wearing them. Second, an aftereffect measure was

defined as the ball’s impact horizontal distance to the target

on the first throw after removing the prisms. Third, an

aftereffect as a percentage of the previous adaptation was

obtained. This last measurement is necessary because each

group can have different adaptation magnitudes, and since

J. Fernandez-Ruiz et al. / Cognitive Brain Research 20 (2004) 92–97 95

the aftereffect is directly correlated with the adaptation, then

a transformation of the raw aftereffect data has to be made

into a percentage of the adaptation. For example, it could

happen that two groups have the same aftereffect magni-

tude, i.e. of 10 cm. But one had an adaptation magnitude of

20 cm, while the other had an adaptation magnitude of 40

cm. If we did not apply the transformation, an aftereffect

comparison would show no differences, while a comparison

of the aftereffect as a percentage of the adaptation would

show the real group differences of 25% vs. 50% of the

adaptation.

3.1.3. Delay

Subjects were divided into five groups of 20 subjects

each. Each group was assigned randomly to a single delay

that could be of 0.1, 1, 5, 10 or 20 min. The delay period

was introduced between the last PRI throw, and the first

POS throw. During delay, the room was completely dark,

and the subjects were asked to stay relaxed with their eyes

closed.

3.1.4. Statistical analysis

In order to compare the different delay groups, a Krus-

kal–Wallis One Way Analysis of Variance on Ranks was

made. This method was chosen because the analysis was

made on transformed data (see above), and not on the raw

data. An all Pairwise Multiple Comparison Procedures

(Student–Newman–Keuls Method) were made to know

the specific differences among groups. The extinction rate

was analyzed by finding the best fit to the averaged data,

and then obtaining the derivatives at different time intervals.

3.2. Results and discussion

Fig. 2 shows the aftereffect at different delays as a

percentage of the aftereffect of the 0.1 delay group. Having

a delay between the last throw while wearing the prism and

Fig. 2. Aftereffect at different delays as a percentage of the aftereffect of the

0.1 delay group. The line represents the best fit using a power function. The

only significant difference found was between delay 0.1 and all other

groups ( p< 0.05).

the first throw after doffing them had a significant impact on

the aftereffect magnitude. In fact a Kruskal–Wallis one way

ANOVA on Ranks showed a statistical difference among

groups (H = 9.95, DF = 4; p < 0.05). A subsequent Student–

Newman–Keuls all pairwise multiple comparison showed

that the 0.1 delay group was different from all the other

groups. No other significant differences were found in the

analysis.

In order to know if delay reduced the aftereffect to levels

similar to the previous baseline magnitude, a paired t-test

comparison between each group’s aftereffect and their

previous baseline was done. The analysis demonstrated that

in all the groups, the aftereffect magnitude was significantly

different from their previous baseline (all p’s < 0.01). A one

way ANOVA on the baseline (PRE) last throw demonstrated

that there were no baseline differences among groups

(F(4,95) = 7; p = 0.59).

To analyze the extinction, the data was fitted to a curve

using specialised software (CurveExpert 1.3, by Daniel

Hyams, Starkville, MS 39759 USA). A Power Fit

( y = axb) was found to had the best fit (r= 0.95) on the

decay data (Fig. 2). The analysis of the regression showed

that the initial decay from 0.1 to 1 min had the major impact

on the aftereffect extinction since the derivatives went from

� 13.5 to � 8.3. The subsequent rate of change was much

smaller, showing a derivative of 0.5, 0.5 and 0.04 for the

measurements made at 5, 10 and 20 min after doffing the

prisms. After the initial minute, the aftereffect decay was

25%, and by 10 min 40% decay had accumulated. In

contrast, the second 10 min (from min. 10 to min. 20) were

characterized by a steady state with almost no extinction rate.

The first throw with the eyes open for both groups of the

first experiment were compared to the aftereffect of the

different groups of the second experiment. The results show

that the 13 throws group is similar to the 1 min delay group

of the first experiment, while the 26 throws group is similar

to the 20 min delay group (t= 1.67, DF = 38; p = 0.1 ns);

since making 13 throws takes less than a minute, the

difference can only be explained by a faster decay in the

26 throws group compared to the 13 throws group.

4. General discussion

The present study addresses two important questions

pertaining procedural memory in general, and prism adap-

tation in particular. First, in the absence of visual reaffer-

ence, does motor reafference information from motor

commands or proprioceptive information affects the spon-

taneous decay observed in passive conditions? And second,

does newly form visuomotor mappings decay spontaneously

in the complete absence of reafference stimulation? The

results obtained in the two experiments suggest that active

motor reafference, in the absence of visual feedback, pro-

duces faster aftereffect decay. The results also suggest that

there is a fast aftereffect extinction component which occurs

J. Fernandez-Ruiz et al. / Cognitive Brain Research 20 (2004) 92–9796

under passive conditions, followed by a more enduring

component that last more than 20 min. Following is a

detailed discussion of these two aspects.

The effect of active motor reafference in the absence of

visual feedback is an important question, since previous

reports tested the same subjects at different time intervals.

Although the subjects were deprived of visual feedback

(by turning off lights, or by occluding vision) the fact that

they were making the same movements was not

acquainted as a possible variable [2,3,7,17]. Here we have

shown that motor activity does produce a faster, but

incomplete, aftereffect decay. It has been proposed that

the aftereffect is the result of the contribution of different

components [2,5]. If, for example, proprioception contrib-

utes to some extent to the total aftereffect magnitude, then

the active movements could specifically contribute to a

faster extinction of that component, resulting in a faster

but partial, decay of the whole aftereffect measurement

[2]. A modular decay has been proven in prism adaptation

using this and other models [5,6]. However, at this point

we have not investigated the possible contribution of

different motor information sources like corollary dis-

charge activity, or proprioceptive information.

The aftereffect decay in the prism adaptation paradigm

has been previously investigated. In an early attempt to

resolve this question, Hamilton and Bossom [22] found a

50% aftereffect reduction in subjects that sat in the dark for

15 min. They tested if the same conditions to establish prism

altered visuomotor mappings were required for returning to

the original mapping, after prism adaptation had taken

place. They specifically tested if visual reafferent stimula-

tion was necessary for the return of the normal coordination.

After their subjects sat in a dark room for 15 min following

adaptation, they were tested again without prisms. The

authors found a significant reduction of the aftereffect,

suggesting to them that the normal visuomotor mapping is

not lost, but is retained and reinstated following prism

removal, even in the absence of any visual feedback. In

the present article, the results from the second experiment

suggest that although there is a passive extinction, a large

component of the aftereffect (60%) persists over 20 min

after training. In another study, Taub and Goldberg [17]

show decay functions for aftereffects during 60 min after

prism removal. The authors report that after 15 min subjects

still had around 40% aftereffects in average, but after 1 h of

testing almost every 5 min, only one of their groups showed

around one fourth of the aftereffect. These results contrast

with those by Dewar [3], who report a much larger afteref-

fect persistence, around 75% after 15 min. Choe and Welch

[2] also found a 50–60% decay of the aftereffect after 15

min, with continuous exposure groups decaying faster than

terminal exposure groups. However, the studies that

obtained decay functions of the aftereffect tested the same

subjects at different time intervals. The present results

provide the first function of the aftereffect extinction rate

not affected by visual or motor reafferences.

Our results suggest that the aftereffect has two compo-

nents: one that shows a fast extinction in the absence of

further visuomotor interactions, and another that shows a

longer endurance. The idea of having two components

with different time ranges has been previously advanced

for explaining changes in the timing of eye–hand coordi-

nation during prism adaptation [15]. It has been argued

that the former component can be strategically used to

quickly correct misalignment, while the later component

would be responsible for slower long-term alignments

[15]. The data showed in the present article suggest that

two different memory processes may contribute to the

aftereffect magnitude, one showing a fast decay mainly

within 1 min, and another that shows a stable endurance

for more than 20 min. The fast decaying component could

be related to motor working memory that depends on

factors like attention, while the second, more stable

component could hold information acquired through pro-

cedural learning mechanisms.

It is interesting to note that although in a typical prism

adaptation/readaptation experiment the adaptation disap-

pears rapidly after removing the prisms, the continuous

training with prisms across several days or weeks result in

the acquisition of a second or even more visuomotor

correlations that can be accessed in the long term

[9,10,21]. The consolidation of a second long-term visuo-

motor correlation suggests that after each complete adapta-

tion/readaptation process some information remains, even if

the subject had already went back to the original baseline

visuomotor performance. We propose that the long-term

component reported in the present experiment is different

from the long-term formation of a second visuomotor

calibration. One important difference would be that the

long-term component we are describing tend to disappear

as soon as the subject starts a visuomotor interaction without

the prisms. In contrast, subjects that have acquired a long-

term second visuomotor calibration can quickly switch

between the old and the new calibrations depending on

different factors like the presence or absence of the prisms

frames [9]. However, it could be possible that some infor-

mation stored during the second component described in

this article could contribute to the acquisition of a long-term

visuomotor correlation of the type obtained through exten-

sive training across many sessions.

It has been previously shown that under normal visuo-

motor reafference conditions complete aftereffect decay can

be observed in less than 1 min of continuous interactions.

Here we have shown that increasing the number of motor

reafferences of the same nature as those used during training

can accelerate the aftereffect decay in the absence of visual

feedback. We also showed that under passive conditions it is

possible to observe two different phases within the afteref-

fect. An initial period is characterized by a fast decay of

about 40% of the total magnitude followed by a second

period in which there is almost no extinction of the

aftereffect.

J. Fernandez-Ruiz et al. / Cognitive Brain Research 20 (2004) 92–97 97

Acknowledgements

We thank Silvia Revuelta and Rafael Ojeda for their help

in testing the subjects. This work was supported by

CONACyT 34817-M, 30970-M and DGAPA IN210300.

References

[1] J.S. Baizer, I. Kralj-Hans, M. Glickstein, Cerebellar lesions and

prism adaptation in macaque monkeys, J. Neurophysiol. 81 (1999)

1960–1965.

[2] C.S. Choe, R.B.Welch, Variables affecting the intermanual transfer and

decay of prism adaptation, J. Exp. Psychol. 102 (1974) 1076–1084.

[3] R. Dewar, Adaptation to displaced vision—the influence of distri-

bution of practice on retention, Percept. Psychophys. 8 (1970)

33–34.

[4] J. Fernandez-Ruiz, R. Diaz, Prism adaptation and aftereffect: speci-

fying the properties of a procedural memory system, Learn. Mem. 6

(1999) 47–53.

[5] J. Fernandez-Ruiz, C. Hall-Haro, R. Diaz, J. Mischner, P. Vergara,

J.C. Lopez-Garcia, Learning motor synergies makes use of informa-

tion on muscular load, Learn. Mem. 7 (2000) 193–198.

[6] S. Kitazawa, T. Kimura, T. Uka, Prism adaptation of reaching move-

ments: specificity for the velocity of reaching, J. Neurosci. 17 (1997)

1481–1492.

[7] S.T. Klapp, S.A. Nordell, K.C. Hoekenga, C.B. Patton, Long-lasting

aftereffect of brief prism exposure, Percept. Psychophys. 15 (1974)

399–400.

[8] A.S. Kornheiser, Adaptation to laterally displaced vision: a review,

Psychol. Bull. 83 (1976) 783–816.

[9] T.A.Martin,J.G.Keating,H.P.Goodkin,A.J.Bastian,W.T.Thach,Thach,

Thach, Throwing while looking through prisms: II. Specificity and

storage of multiple gaze-throw calibrations, Brain 119 (Pt 4)

(1996) 1199–1211.

[10] B.O. McGonigle, J. Flook, Long-term retention of single and multi-

state prismatic adaptation by humans, Nature 272 (1978) 364–366.

[11] G.M. Redding, Visual adaptation to tilt and displacement: same or

different processes? Percept. Psychophys. 14 (1973) 193–200.

[12] G.M. Redding, Decay of visual adaptation to tilt and displacement,

Percept. Psychophys. 17 (1975) 203–208.

[13] G.M. Redding, B. Wallace, Components of displacement adaptation

in acquisition and decay as a function of hand and hall exposure,

Percept. Psychophys. 20 (1976) 453–459.

[14] G.M. Redding, B. Wallace, Adaptive Spatial Alignment, vol. x, Law-

rence Erlbaum Associates, Mahwah, NJ, 1997 194 pp.

[15] Y.K.K. Rossetti, T. Mano, Prismatic displacement of vision induces

transient changes in the timing of eye–hand coordination, Percept.

Psychophys. 54 (1993) 355–364.

[16] L. Squire, Declarative and nondeclarative memory: multiple brain

systems supporting learning and memory, in: P. Andersen (Ed.),

Memory Concepts. Basic and Clinical Aspects, Excerpta Medica,

New York, 1993, pp. 3–25.

[17] E. Taub, L.A. Goldberg, Prism adaptation: control of intermanual

transfer by distribution of practice, Science 180 (1973) 755–757.

[18] E. Tulving, Human memory, in: P. Andersen (Ed.), Memory Con-

cepts. Basic and Clinical Aspects, Excerpta Medica, New York,

1993, pp. 27–45.

[19] M.J. Weiner, M. Hallett, H.H. Funkenstein, Adaptation to lateral dis-

placement of vision in patients with lesions of the central nervous

system, Neurology 33 (1983) 766–772.

[20] R.B. Welch, Perceptual Modification: Adapting to Altered Sensory

Environments, vol. xv, Academic Press, New York, 1978 346 pp.

[21] R.B. Welch, B. Bridgeman, S. Anand, K.E. Browman, Alternating

prism exposure causes dual adaptation and generalization to a novel

displacement, Percept. Psychophys. 54 (1993) 195–204.

[22] C.R. Hamilton, J. Bossom, Decay of prism aftereffects, J. Exp. Psy-

chol. 67 (1964) 148–150.