Progressive improvement in discriminative abilities in adult owl monkeys performing a tactile frequency discrimination task.

JOURNALOF NEUROPHYSIOLOGY Vol. 67, No. 5, May 1992. Printed

in C!S...-i.

Progressive Improvement in Discriminative Abilities in Adult Owl Monkeys Performing a Tactile Frequency Discrimination Task GREGG H. RECANZONE, WILLIAM M. JENKINS, GARY T. HRADEK, AND MICHAEL M. MERZENICH Coleman Laboratory and Keck Center for Integrative Neurobiology, Departments of Physiology and Otolaryngology, University of California, San Francisco, California 94143-0732 . SUMMARY

AND

CONCLUSIONS

I. Adult owl monkeys were trained to detect a difference in the frequency of sequentially applied tactile stimuli presented to a constant, restricted location on the glabrous skin of a single finger. Psychophysical performance functions and thresholds were determined on daily sessions over a 3- to 20-wk-long training period. 2. Thresholds for the trained digit progressively decreased from a 6- to ~-HZ difference to a 2- to ~-HZ difference relative to a 20-Hz standard. These thresholds were similar to those described for macaques and humans determined by the use of a two-alternative forced-choice procedure. 3. Six of the seven studied monkeys showed a continuously progressive improvement in performance with training. Early in the training period, the performance improved at about the same rate for all frequencies. Later in the training period, the performance for frequencies much greater than the comparison frequency improved sooner than did the performances for frequencies more similar to the comparison frequency. This resulted in an increase of the slope of the psychometric function near threshold. In a single monkey, no clear later-component improvements were recorded. 4. Analyses of performances using the theory of signal detection revealed a progressive increase in the measure of d’ for all frequencies above threshold. 5. Some improvements in performance were also recorded when stimuli were applied on an adjacent digit, which was trained for 2 or 3 sessions spaced throughout the course of training. However, thresholds on these digits were always greater than those on the trained digit. These findings suggest that there are local changes generated by this training at somatotopically restricted regions of the central somatosensory nervous system. 6. It is concludedthat this training resultedin a genuineprogressiveimprovement in temporal acuity specificto the trained skin. The initial rapid improvement waslikely dueto an improvement in the “strategy” or “cognitive” aspectsof the task, whereas moregradualimprovementsin performancerecordedthroughout the training period were most probably due to somatotopically localizedchangesin the neural representationsof the behaviorally relevant stimulus.

INTRODUCTION

Experiments conducted within the past 15 years provide unequivocal evidence that the distributed response properties of neurons in the adult cerebral cortex are mutable. Several studies have described changes in the topographic representations in the cortex after alterations of peripheral inputs. In studies of the primary somatosensory cortical fields, these experimental manipulations have included deafferentation (Calford and Tweedale 1988, 199 1; Franck 1980; Kalaska and Pomeranz 1979; Kelehan and Doe&h

1984; Merzenich et al. 1983a,b, 1984; Rasmusson 1982; Wall and Cusick 1984), surgical fusion of digits (Allard et al. 199 1 ), neurovascular island transfer (Clark et al. 1986), and behaviorally controlled differential stimulation (Jenkins et al. 1990; for recent reviews see Kaas et al. 1983; Merzenich et al. 1988, 1990). Some parallel studies have also been conducted in the primate second somatosensory cortex (Pons et al. 1988), the rat motor cortex (Sanes et al. 1990), the guinea pig primary auditory cortex (Robertson and Irvine 1989), and the cat striate cortex (Kaas et al. 1990). In addition to the alteration in the topographic representation of the sensory epithelia as defined by “mapping” studies, a number of experimental paradigms have demonstrated that the distributed neuronal response properties of cortical neurons can be substantially remodeled by behaviorally relevant stimuli. For example, several studies have been conducted by recording from single cortical neurons during the presentation of specific stimuli after behavioral conditioning (Buchhalter et al. 1978; Diamond and Weinberger 1986; Disterhoft and Olds 1972, Disterhoft and Stuart 1976; Kitzes et al. 1978; Kraus and Disterhoft 1982; Olds et al. 1972; Oleson et al. 1975; Woody et al. 1976; see also Delacour et al. 1987; Fregnac et al. 1988; Iriki et al. 1989; Miyashita 1988; Miyashita and Chang 1988; Rolls et al. 1989; Sakamoto et al. 1987). Experiments conducted in which stimuli are presented in a behavioral context have shown that a major percentage of studied neurons in appropriate sensory or motor cortical areas are differentially engaged by the behaviorally relevant stimulus in an awake animal. This implies that the training results in a substantially increased neural representation of that “important” stimulus. These clear demonstrations that the distributed response properties of cortical neurons in adult animals are alterable raise the issue of the perceptual consequences of lesion- or training-induced changes. One possibility was suggested by studies of human amputees (see Cronholm 195 1; see Henderson and Smyth 1948; Teuber et al. 1949). Nearly all amputees experience the illusion of a “phantom limb.” In most cases, the phantom “telescopes,” i.e., the amputated arm is perceived to shorten over time, resulting in the illusion that the phantom hand approaches the stump (Henderson and Smyth 1948 ) . Amputees had improved performance on psychophysical tests of two-point discrimination, absolute location, and sensation threshold when the stimuli were applied to the stump skin as compared with when the stimuli were applied to the homologous skin of the contralateral arm, or of normal individuals (Haber 1958; Teuber

0022-3077/92 $2.00 Copyright 0 1992 The American Physiological Society

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1016

G. RECANZONE,

W. M.

JENKINS,

G. HRADEK,

AND

M.

M.

MERZENICH

et al. 1949). These clinical and psychophysical observa- changes in the somatosensory system? 2) How are the topotions are consistent with 1) a partial conservation of the graphic representations of the hand in cortical areas 3a and representation of the missing limb in the cortex, which ac- 3b of an adult primate altered as a result of this animal’s counts for the phantom; and 2) an occupation of the arm or learning a stimulus discrimination task through repetition? leg representation by an expanded representation of the 3) Does the behavioral relevance of a stimulus influence the stump skin, which accounts for the perceptual foreshortenchanges that occur in the cortex? ing of the limb, the increased acuity, and the increased sensiThe somatosensory cortex in adult owl monkeys has protivity of this skin area. These interpretations remain valid vided the most experimental evidence of cortical plasticity, with consideration of the limited reinnervation of the and this model system has been used for these studies. The stump skin and in cases of neuroma formation. This expla- strategy was as follows: I) to train adult owl monkeys to nation was first proposed by Teuber and colleagues and discriminate frequency differences between successive tacelaborated by Merzenich et al. ( 1984). tile stimuli applied to a constant, restricted finger location; in behavioral perforA second potential example of the perceptual conse- 2) to document the improvements quences of functional cortical reorganization with experimance with training; 3) to define the spatial and temporal ence is the phenomenon of learning with training. Training response properties of cortical neurons representing the a human or animal in a specific perceptual/ behavioral task trained skin; 4) to compare these distributed neural reinvolving a restricted sensory input and a specific motor sponses with those of cortical neurons representing equivaoutput results in a stimulus-dependent improvement in the lent but untrained skin surfaces; and 5) to compare these performance at that task. This type of learning has been responses with those of cortical neurons representing equivobserved in virtually all sensory modalities and applies to a alently stimulated but untrained skin surfaces. This report wide variety of motor behaviors (for reviews see Anderson describes the results of the psychophysical study. 1980; Fitts 1964; Gibson 1953; James 1890; Singley and Several investigators have studied the responses of priAnderson 1989; Volkmann 1858). William James hypothmary afferents to a narrow range of tactile stimuli to define esized that an alteration of the distributed “excitability” of the specific inputs that represent those stimuli that are availthe cerebral cortex could account for this phenomenon able to the CNS. For example, Mountcastle and colleagues (James 1890). Sherrington and colleagues provided the have studied the responses of peripheral afferents innervatfirst experimental evidence that the cerebral cortex could be ing the glabrous surface of the hand and central neural refunctionally reorganized in the adult mammal (Graham sponses to tactile stimuli in the flutter-frequency range ( loBrown and Sherrington 19 11; see also Graham Brown 50 Hz) (Mountcastle et al. 1969, 1990; LaMotte and 19 15 ). The concept of “the (location-specific) mutability Mountcastle 1975, 1979). These studies indicate that of the cortical point” was raised by Sherrington and col- quickly adapting cortical neurons that receive their primary leagues (Graham Brown and Sherrington 19 12) and hy- input from the Meissner’s corpuscles in the glabrous skin pothesized by them to underlie the acquisition of motor are the most likely to account for frequency discrimination skill. behavior in the range of lo-50 Hz, whereas the response of It has become apparent that both representational and slowly adapting cortical neurons better represent the intenperceptual plasticity resulting from peripheral lesions or sity of the stimulus independent of the frequency in this training could be manifestations of the same dynamic neu- range (Talbot et al. 1968; see also Gardner and Palmer rological processes. Several hypotheses have been proposed 1989a,b; Mountcastle et al. 1969, 1972, 1990). Experito account for the dynamic response properties of cortical ments in SI cortex showed that the amplitude of the tactile neurons that are based on distributed, behaviorally signifistimulus that corresponded to the psychophysically defined cant, temporally coincident activity (Edelman 1978, 1987; detection threshold correlated with the amplitude of the Merzenich et al. 1988, 1990; von der Malsburg and Singer threshold for single neurons in SI (Mountcastle et al. 1969, 1988; Singer 1990). The temporally based alterations of 1990), whereas the amplitude thresholds at which fresynaptic strengths in conjunction with changes in effective quency discriminations could be made approximately corticocortical interactions could plausibly account for the corresponded to the amplitudes at which single cortical neuthree classes of observations noted above (see Merzenich et rons fired at least one action potential for every stimulus cycle. Increasing the amplitude further did not significantly al. 1988, 1990). Stimulus-driven changes in somatotopic maps have been demonstrated after behaviorally controlled affect the discriminability of the stimulus. Psychophysical differential stimulation (Jenkins et al. 1990). These au- studies and microneurography experiments on human subthors demonstrated that mechanical stimulation of a re- jects are consistent with these observations ( Torebjork et al. stricted skin location in a behavioral task in which the ani1980, 1987; Vallbo et al. 1984). mal was required to maintain contact with the stimulus These studies led to three important conclusions. 1) The resulted in “locally expressed” changes in the somatotopic tactile frequency discrimination of humans and macaques representation of the stimulated skin in area 3b. However, were roughly equivalent. 2) Single cortical neurons in SI up to this time there is little direct evidence that the cortical could fire action potentials at every stimulus cycle for frerepresentation of a given sensory surface is altered by experiquencies in the flutter range ( lo-50 Hz). 3) The stimulus ence in parallel with experience-driven differences in per- intensities at which SI neurons would respond by cycle-forceptual acuity. cycle firing occurred at the stimulus intensities at which the We sought to address these issues directly by asking the frequency could be discriminated. It is of interest to know if following questions. I) Are improvements in performance the discrimination performance would increase for a skin in a stimulus discrimination task attributable to local location if the discrimination was practiced at that particu-


TACTILE

FREQUENCY

DISCRIMINATION

lar location over several thousand trials. If improvements in performance do occur selectively for “trained” skin, distributed neural responses could then be compared between the trained skin and an analogous area of skin that was not trained and that therefore had a higher discrimination threshold. The differences in discriminability would be represented by a specific difference in the topography and/or in the temporal resolution of the stimulus within the cortical representation of the trained skin, when compared with homologous skin that was not trained in the behavioral task. In this report we describe the psychophysical results of adult owl monkeys that were trained to discriminate differences in the frequency of a flutter-frequency stimulus when compared with a 20-Hz standard stimulus. These stimuli were all above amplitude thresholds for detection and discrimination and presumably engaged a restricted area of afferent receptors in the glabrous hand to respond with discharges entrained to the stimulus frequency. The frequency discrimination abilities of these animals were defined in daily training sessions over a period of weeks. The performance at the trained skin location was compared with that of an equivalent skin location on an adjacent digit derived in two or three sessions during the course of training. The following reports describe the electrophysiological experiments conducted on these same animals in somatosensory cortical areas 3a and 3b (Recanzone et al. 1992a-c). METHODS

.4nimals Feral adult owl monkeys of both sexeswere usedin all experiments.They wereindividually cagedwith free accessto water and weremaintainedon a reverse12-hlight /dark cycle with the lights coming on at 7:00 pm. Carewastaken to ensurethat the animals werein goodgeneralhealth throughout the courseof the study. All methodologicalproceduresregardingthe care and use of these experimentalanimalsfollowedthe guidelinesof the National Institutes of Health for the care and use of laboratory animals.

PLyychophysical procedure The psychophysicaltraining and testingprotocol hasbeenpreviously describedin detail ( Recanzoneet al. 1991). Animals were trained to discriminatethe frequency of a sinusoidaltactile stimuluspresentedto a restrictedskin regionof a singledigit. The stimulated skin region compriseda smallpart of a singlesegmentof a singledigit. This wasaccomplishedby training the animal to place Correct Hand Contact

AL, UN

False-Positive

OFF-

CM 9

Lights

OFF

L - %

Contact Light

ON

Reward Light

ON OFF

Reward

ON OFF

II

*

N

Tactile Stimulus .

a G fvl~s~ime-out

.----

OFF A

II

.

CI

False-Positive Time-Out

w

I

1017

it’s hand onto a speciallydesignedhand mold with five shallow grooves,one to accommodateeachdigit. Six gold-platedfoil strips wereplacedon the mold, one correspondingto eachdigit and one to the palm. The monkey completed a high-resistancecircuit by contacting thesefoil stripswhile standingon the cagefloor. A trial did not begin until the monkey contacted thesefoil strips,which could only be doneby a single,unique hand positionon the mold. The stimulus probe contacted the skin from below, through an openingin the mold. The invariant location of the stimulusprobe and the requirementthat the animal’shand be placedon the mold in the sameposition for eachtrial ensuredthat the stimulusprobe contacted the skin at the samelocation on eachtrial. Analysis of videotaped sessions with the cameramounted directly above the hand mold wasdone to determinethe variability of the hand placementand, thus, of the stimulusprobe location. The position of eachknuckle wasmarkedon an acetateoverlay on the video monitor for 500-l ,000 trials over the course of 3-5 sessions scatteredacrossthe training period for eachanimal. The greatestvariation of knuckle position on the stimulateddigit was measuredasa radius of co.75 mm, with ~90% located within a radiusof 0.5 mm. This resultedin an absolutemaximum areaof skin stimulatedby the tactile probeover the courseof training not exceeding3.5 mm diam, with the vast majority of contactsbelow that measure. The tactile stimulator wasa servo-controlledmechanicaltransducer ( Chubbuck 1966) operated in a controlled-displacement mode. The stimulus probe was2 mm diam with a rounded tip. The displacementof the sinusoidalstimuli for all but control trials was 300 pm peak to peak, superimposedon a rampeddisplacement. The stimulusprobe did not contact the skin before a trial wasinitiated. The contact force with the skin during presentation of the sinusoidalstimuluswas6- 10g in different individual monkeys. Inter-individual variability was attributed primarily to the monkey’shandgeometry.Theseforceswereconstantin eachindividual monkey and did not changeover the courseof training and testingeither within or betweensessions. A schematicdiagramof the psychophysicalprocedureis shown in Fig. 1. Eachtrial wasinitiated by the animalcorrectly placingits handon the mold (seeabove). After a 1-spre-period,the stimulus probe was ramped onto the skin. The probe was then vibrated sinusoidallyat 20 Hz for 650 ms,followed by a 650-mspause.One to five subsequentburstsof stimuli were presentedon the same schedule.On one of thesesubsequentbursts,the frequencyof the stimuluswas~20 Hz ( S2). The animal wasrequired to maintain contact throughout the presentationsof the 20-Hz stimulus(S 1) and to break contact when the frequency of the tactile stimulus was~20 Hz (S2). Correct responses were rewardedwith a 45-mg food pellet. A correct responsecould be madeduring an 800-ms rewardwindow that began150msafter the onsetof the S2stimulus. Responsesto a 20-Hz stimulus (False-Positives)or no responseto the S2 (Misses)were penalizedwith I- to 5-stime-outs. Miss

F

IN OWL MONKEYS

%

FIG. 1. Schematic diagram of the behavioral paradigm. The animal initiated each trial by making “correct” contact with the hand mold, which placed the tactile probe onto an invariant location on the skin. After a preperiod the stimulus probe was ramped onto the skin and presented as 650-ms pulses of sinusoidal stimulation, superimposed onto this ramped displacement. Stimulus bursts were interrupted by 650-ms pauses. The frequency of the stimulus pulsein bins 2-6 was pseudo-randomly selected to be a greater frequency, S2. A correct response was to break correct hand placement within an 800-ms reward window, which began 150 ms after the onset of the S2. All correct responses resulted in the brief illumination of the reward light and the delivery of a food reward. False-Positive responses ( 1st broken arrows)resulted in the termination of a trial and a brief time-out in which the house lights were extinguished. Miss responses also resulted in a time-out.


G. RECANZONE,

1018

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M.

JENKINS,

G.

The stimulus burst in which the S2 frequency was presented was pseudo-randomly determined to occur in bursts 2-5. If the animal did not make a response to this stimulus, the probe was withdrawn from the skin, and a brief time-out followed. The probability of an S2 occurrence in any given stimulus burst ( -0.388) was set such that it did not change during the course of a single trial. To accomplish this, it was necessary to present the S2 frequency in the sixth burst on a significant number of trials. These trials were considered “catch” trials, because in all cases in which a stimulus was presented in the sixth burst, it was the S2 frequency. These trials were omitted from the determination of performance. Three to six months of training were required before psychophysical thresholds could be derived. Animals were first trained to make appropriate hand contact with the mold by successive approximations. The next stage required the monkey to maintain contact with the mold for a variable period of l-5 s and to release the mold on detection of a high-amplitude,40-Hz stimulus.The S1stimuluswasthen introduced by the useof a fade-intechnique, with the initial parametersbeing loo-pm displacementand ~-HZ frequency. The Sl stimuluswasgradually increasedin amplitude and frequency to match that usedin the final task, and then the amplitudeof the S2stimuluswasreducedin amplitudeto 300 pm and reduced in frequency to the range used in testing. Fully trained animals were tested 6 days a week, receiving 500-700 trials/day ( 1,500-2,100 stimulusbursts/session).Six to 10different S2 frequencies,one of which wasalwaysbelow threshold(see below), were eachpresentedon 20-50 trials/session.

Data analysis Three categoriesof responsewereusedfor the calculation of the monkeys frequency discrimination performance. I) Hit: the responsewasmadeduring the S2 presentationin bins2-5. Each S2 frequency wascounted independently. 2) Miss: no responsewas madethrough the presentationsof S1or the rewardwindow for S2 presentationsin bins2-5. EachS2frequencywascountedindependently. 3) False-Positive:the responsewasmadebeforethe reward window but after the onsetof the secondSl presentation. Two other responsecategorieswere recorded,but the responses on thesetrials were not used to calculate performance because they occurred in stimulus presentation bins for which the frequency wasnot randomly determined. 1) Pre False-Positive:the response wasmadebeforethe onsetof the secondstimuluspresentation, either Sl or S2. The frequency of the stimulusin bin 1was always20 Hz. 2) Catch: correct hand position wasmaintainedto the last stimuluspresentation(bin 6). The animal wasrewarded with a releaseor punishedwith a Miss time-out if there wasno release.The S1stimuluswasnever presentedin the sixth presentation bin.

HRADEK,

AND

M.

M.

MERZENICH

comparablewhen the animal was under stimulus control. The total False-Positiverate for the session,Fp,, wasthen derived by FP,

= ( no. of responses to S 12-5)/( no. presentations of S 12-5)

where the subscriptcorrespondsto the bin of stimuluspresentation. To calculate the performance rate (P), the Hit rate was corrected for by the False-Positiverate. The correction factor was the Safe period rate (S), which was defined as ( 1 - FP). The overall performancerate for a given S2 frequency ( Ps2) wasthen calculatedas ps2

= St- K 1 -

Hs2)

x &I

which reducesto Ps2 = HQ x s,

The resultof this equation goesto H asSgoesto 1 (no False-Positives) and goesto 0 asS goesto 0 (all False-Positives). The performanceat eachS2 frequency wascalculatedwith correction for the False-Positiverate. Threshold was taken as the frequencythat the animal discriminatedfrom 20 Hz on 50%of the trials. In a few sessions in each animal, the tactile stimulator was positionedto contact the homologousskin surfaceon an adjacent digit. Thresholdswere derived on this digit in the samemanner.

Chance performance/catch

trials

Chance performancecan be calculated asthe probability that the next stimuluswill be the S2 ( -39%) multiplied by the probability that the animal will make a responsein the absenceof an S2 (the False-Positiverate). This value is 1.9-5.7% for False-Positive ratesof 5 and 15%,respectively.One empirical method of determining chanceperformanceis to presenta 20-Hz “S2” stimulus. This wasdone at a probability of 1:50- 1:100in eachsession.The performance averagedover many sessions for thesecatch trials werein good agreementwith the calculatedvaluesfor all studied monkeys. Catch trials were also run for each monkey to eliminate the possibility that there was an external cue that could signal the presentationof the S2 stimulus. In IO-20 trials presentedin 3-5 sessions for eachmonkey, the tactile probewasmoved sucht!lat it could not contact the skin. Animals never respondedto the presentation of the S2 in thesecontrol trials.

Calculation

of d’

Principlesof signaldetection theory were usedto calculatethe value of d’ for eachS2 frequency for eachtraining session(Green and Swets 1966). The d’ value was derived by calculating the z-score for ( 1 - H) and subtracting from it the z-scorefor ( 1 FP). In the instancesin which the Hit rate was 100%for a given Threshold determination frequency,the z-scorefor ( 1- H) wasassigneda value of 3.0. This The determination of thresholdfor any sessionwasdependent resultedin a d’ at frequencieswith Hit rates of 100%that were on 1) the Hit rate at eachpresentedS2, and 2) the False-Positive >3.0. rate measuredover the session.The Hit rate for a given S2 frequency was defined from data pooled from runs in which the Statistical analysis given S2 frequency waspresentedin bins 2-5 by the equation All statisticalanalysiswasdone on a Macintosh computer with the useof the softwareStatview 5 12+. The specificstatisticaltest Hs2 = (no. correct responses)/( no. stimulus presentations) usedis describedin the text and/or figure legends,whereapproThe False-Positiverate wasdefinedasthe rate at which a response priate. P values~0.0 1 weretaken asbeingstatistically significant. wasmadeto the S1 stimulus(Fp). This value wasderived for each stimulusbin aswell asfor the overall rate acrossbins.For eachbin RESULTS fi’P, this value wasderived by

Thresholds

FP,l

= (no. of responses to Sl in bin n)/( no. Sl presentations in bin n)

Seven monkeys were trained on the tactile discriminafor 2 1- 13 1 consecu-

The False-Positivevalues of each presentationbin were always tion task. Thresholds were determined


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tive days from the first session in which thresholds were derived in these animals. Six animals could eventually detect a difference in frequency on the trained digit of -2-3 Hz relative to the 20-Hz standard (range, 1.53-2.87 Hz). The behavioral thresholds, expressed as the mean threshold measured over three consecutive sessions for the trained skin, are summarized in Table 1. These values, when considered as a percentage of the 20-Hz comparison stimulus, were ultimately on the order of 10% for the trained digit, and 20% for the adjacent, untrained digit.

E-l

Improvement

E-2

in performance

Six of the seven animals studied on the tactile frequency discrimination paradigm showed a clear improvement in performance with training. Thresholds that were determined at three different stages of training are shown in Table 1. The initial stage was defined as the first three sessions in which thresholds < 10 Hz were obtained. The final stage was defined as the last three consecutive sessions, and the middle stage was the midpoint between these two extremes. In six of these seven monkeys (excluding monkey E4) the thresholds progressively decreased over these three periods. All monkeys had similar thresholds at each of these three periods of training, even though they constituted very different durations of training ( range, 2 1- 131 consecutive days). The mean initial threshold for all monkeys was 6.48 Hz. This value excludes the initial threshold for digit 4 of monkey Et5 for reasons described below. The mean middle threshold for all monkeys except E4 was 3.27 Hz, which is -50% of the initial threshold. Monkey E4 is omitted from the calculation of the mean for the middle and final threshold values because this monkey did not show a significant improvement in performance by any measure (see below). Finally, the mean final threshold was 2.20 Hz, which equals 36% of the initial threshold and 72% of the middle threshold. When considered across monkeys, excluding the specific cases noted above, the thresholds taken at these three TABLE I.

Monkey El E2 E3 Ii-4

ES Et%03

Et%04 E7

Mean

Summaryof . thethresholdsdejned on the trained digit Initial Training Sessions 6.43 9.85 6.68 7.28 7.04 5.29

-t 0.17 AI 1.64

zk0.57 IL 2.28 2 0.45 + 0.09 2.63AI0.25 5.22 + 1.84 6.48 IL 2.30

Middle Training Sessions 3.89 3.79 4.68 5.74 3.11 2.84

+ 0.21 + 0.14 + 0.21 + 0.84 2 1.74

k 0.52

2.17t 3.30 3.27

+

0.30 0.34

I!X 1.10

Final Training Sessions

Ik 0.25 * 0.14 + 0.24 k 5.5 + 0.7 1 -t 0.07 I!I 0.21 AI 0.19 2.20+ 0.50

1.95 2.22 2.69 7.84 2.20 1.62 1.53 2.87

Total Number of Training Sessions 58

131 110 80 30

37 21 75

0

20

40

60

80

100

0

20

40

60

80

100

120

E-4

~O!~:~:~:~:~:~:~:~’ 0

20

40

60

80

Day FIG. 2. Thresholds plotted as a function of consecutive days of training. Day I is taken as the 1st day a delta frequency was presented in which the performance was ~50%. Data are presented only from sessions in which both the False-Positive rate was < 15% and there were at least 20 presentations of an S2 stimulus below threshold. Filled circles denote thresholds determined on the trained digit, and open squares denote thresholds determined on the adjacent, untrained digit. The comparison frequency was 20 Hz in this and all figures. Bold type letter-number combinations refer to the individual monkey ( see Table 1). A-C: from 3 representative monkeys that showed improvement in performance with training. D: from the single animal that did not improve in performance.

epochs in time were statistically significantly

different from

Values are means + SD. Thresholds are taken for 3 consecutive days of each other (one-tailed unpaired t test, P < 0.00 1). training. Initial training sessions are the 1st 3 days of training in which Figure 2 shows the threshold, defined as the difference in thresholds < 10 Hz were derived. Middle training sessions are the 3 sessions beginning at the midpoint of the total days of training. Final training ses- frequency (delta frequency, Af) at which the animal persions are the final 3 sessions of the training period for that monkey. Mean formed at 50% correct, plotted as a function of consecutive was calculated from the 3 threshold values for each monkey. Case E6-D4 was omitted from analysis of the mean of the initial values; case E4 was days for three representative monkeys, the performance of which improved (A-C), and for the one animal in which omitted from calculation of the mean for the middle and final training sessions. See text for explanation. performance did not improve (0). The improvement in


G. RECANZONE,

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W. M. JENKINS,

G. HRADEK,

performance was rapid over the first lo-20 sessions. This early time period showed the most variation in threshold between consecutive days (e.g., animal E3, Fig. 2C). The rate of improvement became more gradual over the next several weeks to months. This later period was marked by much smaller variations of the threshold measured between sessions. One clear exception to this general observation was recorded in animal E4 (Fig. 2 D, Table 1). This animal never performed consistently at the smaller delta frequencies, leading to a consistently large variability in threshold measurements. The psychometric functions for five different sessions taken throughout the course of training in a representative monkey (E2) are shown in A-E of Fig. 3, with these functions shown together in Ffor direct comparison. The performance at high frequencies (S2 > 28 Hz) improved to near perfect levels over time, with little intersession variability in performance. The performance at frequency differences closer to threshold, however, revealed a more sequential improvement. For example, the improvements at Afs of 6 and 8 Hz were greater than at 5 Hz between sessions 3 and

B

#3

AND M. M. MERZENICH

48 (see Fig. 3 F). The improvements at Afs of 4 and 5 Hz were greater than for 3 Hz between sessions 48 and 88, similarly the improvements at Afs of 4 and 3 Hz were greater than at 1 and 2 Hz between sessions 88 and 122. This sequential improvement in performance at different frequencies was seen in each of the six monkeys that showed an overall improvement in performance. As shown in the representative example in Fig. 3, this was reflected by an increase in the slope of the psychometric function near threshold. The slope of the psychometric function was defined as the slope of the line connecting the data point that was just above 50% performance with the data point that was just below 50% performance. The means and standard deviations of these slopes for the first three sessions (O), for the middle three sessions (middle as defined in Table 1, and for the last three sessions ( l ) are shown for all studied monkeys in Fig. 4. In all but one case (E4), these slopes progressively increased during the course of the training period. This progressive improvement in frequency discrimination performance is shown in another way by plotting the

#18

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16 14 12 10 8 6 Delta Frequency C 1.0

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16 14 12 10 8 6 Delta Frequency

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#48

T FIG. 3. Representative performance functions taken during 5 different training sessions in 1 representative animal (E2). The performance at each S2 frequency is plotted on the y-axis. The delta frequency, defined as the difference in frequency between the S2 and the 20-Hz comparison, is plotted on the x-axis. The dashed line is drawn through a performance of 50%, which was defined as threshold. A-E: taken from the different training sessions noted above each graph. F: composite of A-E.

a> 0.8 E cd 0.6 E ,o & 0.4 CL

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16 14 12 10 8 6 Delta Frequency 1.0 T

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TACTILE

70 60

0 Initial Training Sessions @ Middle Training Sessions l Final Training Sessions

1

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sessions 93 and 109, and only a 16% decrease in the threshold on the adjacent digit. The performance functions for both digits are shown for each session in which the adjacent digit was tested in a representative example (monkey E3) in Fig. 6. In each case, the performance function of the trained digit was plotted with the performance function of the untrained digit on the next day. Discrimination on the trained digit was consistently

t

30 Hz 1 go.8 O!

I El

I E2

I E3

I E4

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performances at particular frequencies across sessions (Fig. 5 ). This representative animal first improved at 30 Hz on session 2 (Fig. 54); at 26 Hz the performance improved above 50% after 48 sessions (Fig. 5 B); at 24 Hz the performance improved on session 79 (Fig. 5C). This animal (E3) never consistently performed above the 50% level at 22 Hz ( Fig. 5 D). Similar results were seen for all of the other cases in which performance substantially improved. Performance with stimulation adjacent digit

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In each animal an adjacent digit was tested by the use of the same behavioral paradigm ( open squares, Fig. 2) in two or three single sessions. Frequency discrimination thresholds for stimuli presented on the adjacent digit were in every case greater than were the thresholds determined on the preceding and following sessions for stimuli presented to the trained digit. Table 2 shows the comparison for all thresholds derived on the adjacent digit. In all monkeys the thresholds on the adjacent digit were determined during the final stages of training. At this period the difference was always more than two standard deviations greater than the threshold measured on the trained digit. In three monkeys, thresholds were also derived earlier in training (monkeys El, E2, and E3). This difference was not always as great earlier in training, and in some cases the threshold on the adjacent digit was equivalent to the threshold on the trained digit (e.g., E2, session 65 ) . The improvements in performance on the adjacent, untrained digit did not appear to match that of the trained digit. For example, the threshold on the trained digit decreased by 30% between sessions 44 and 55 in monkey El, whereas the threshold on the adjacent digit slightly increased over that same period. For monkey E2, the threshold on the trained digit decreased by 44% between sessions 65 and 128, whereas the threshold on the adjacent digit decreased only 22%. Finally, monkey E3 had a 34% decrease of the threshold on the trained digit between

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1022

G. RECANZONE,

W. M. JENKINS, G. HRADEK,

2. Thresholdson the trained digit und an acr(jacent, untrained digit TABLE

Monkey El

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Session Number 30 44 55 65 128 35 93 109 37 78 28 73

Trained Digit Threshold 3.89 2.79 1.95 3.94 2.22 4.28 4.06 2.69 5.24 7.85 2.20 2.87

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Adjacent Digit Threshold 4.75 3.50 3.75 3.96 3.10 7.24 5.17 4.34 8.55 7.67 6.22 3.50

Adjacent/ Trained* 1.22 1.25 1.92t 1.01 1.40t 1.69 1.27 1.617 1.63 0.98-t 2.83t 1.22-f

AND M. M. MERZENICH

sessions similar to those in successfully trained animals (see Table 1). The performance at large Afs (for example, 8 and 10 Hz) did improve, and the animal performed well at these large frequency separations. Note that in contrast to other trained monkeys, this one monkey’s performance functions did not change in slope over time (see Fig. 4). The psychometric functions shifted along the x-axis. The only apparent improvement over time was for 26 Hz between sessions 34 and 58. The perfor-

’ .‘T

Values are means + SD. Thresholds on the training digit are of 3 consecutive sessions beginning on the session indicated (Session Number). Thresholds on the adjacent digit are taken in a single session (Session Number). Monkey E6 is not included in this table as both digits 3 and 4 were extensively trained. *Ratio of the threshold derived on the adjacent digit divided by the mean threshold derived on the trained digit. tRatios taken for the final training sessions.

Untrained mr

better than on the untrained digit for all but the highest frequency differences. There did appear to be some modest improvements with training conferred on the adjacent digit. It should also be noted that the False-Positive rate was approximately equal regardless of which digit was being stimulated. The improvements in performance and the transference of some gains to the adjacent digit is illustrated for one monkey that was sequentially trained on both digits (Fig. 7). The thresholds derived on digit 3 are shown as filled circles, whereas those from digit 4 are indicated by open squares. As in other cases, frequency discrimination thresholds clearly decreased over the course of 44 days on digit 3, with initial rapid improvements and subsequently more gradual improvements. On day 45, the tactile probe was moved to digit 4. The threshold at this untrained skin site was initially about twice that on the trained digit 3 (see Table 1)) but the performance at this new site also progressively improved over the course of the next 20 days. At the end of this period, the threshold on digit 3, which had not been stimulated in this task over the preceding 20 days, was tested again. The frequency discrimination threshold was again increased to a level comparable with that of the pretraining value derived on digit 4 (3.75 vs. 3.90 Hz).

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The performance functions in Fig. 8 illustrate some of the results from the only monkey that did not improve in performance with training (E4, Fig. 2 D). This animal would consistently make correct responses for large frequency differences ( 12-20 Hz), but the behavior degenerated to a guessing strategy once the task became more difficult. Thresholds remained highly variable between sessions. Representative examples of the performance functions of this animal over time are shown in Fig. 8A. The performance at frequencies ~25 Hz never improved above threshold, even though this animal had a total number of training

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TACTILE

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mance on the adjacent digit was tested on day 37 (Fig. 8 B) and was clearly worse in performance when compared with the trained digit measured the previous day. Later in training, this difference was not as dramatic and may be a reflection of the highly variable differences in threshold observed in this one monkey. I

Analysis by theory of signal detection The results expressed by simply plotting the threshold defined for each session as a function of training suggests an improvement in the frequency discrimination ability for stimuli applied to that specific skin region. Signal Detection Theory (Green and Swets 1966) models a subject’s performance as setting a criteria level between two partially overlapping distributions: a hypothetical “signal” distribution and a “signal-plus-noise” distribution. The model assumes that these two distributions are Gaussian in shape and have equal variance. The difference between the two peaks in these distributions are expressed in units of variance as the value d’, where complete overlap gives a value of 0, and no overlap is achieved at a value of 3. d’ values of 1 ( 1 standard deviation separation) are generally taken as threshold. This method has an advantage in that it is not dependent on the subject’s internal “criteria” by which it makes a response. Improvements in performance may occur in two ways according to signal detection theory. 1) The monkey could change it’s criteria so that it makes more “Hits” but also more “False-Positives.” In this case, no improvement of discriminability has actually occurred, and the signal and signal-plus-noise distributions remain the same. The value of d’ would not change. 2) The discrimination performance of the monkey could improve by increasing the separation of the two distributions. This true increase in perceptual acuity would result in an increase in d’. Three observations in the behavioral data demonstrate that the discrimination performance improved on the

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trained skin in all but one of the trained monkeys. First, the individual performance functions changed in slope with training (see Figs. 3,4, and 6). If these monkeys were only changing criteria, these performance functions would simply move along the x-axis. Second, the data used in calculation of the behavioral performance were only taken from sessions in which the False-Positive rate was cl 5%. The mean and standard deviation of the False-Positive rates for each animal over all sessions in which performance data were derived is shown in Fig. 9. If the improvement in pera 5o 12 40 g p 30 z% 20

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1024

G. RECANZONE,

W. M. JENKINS,

G. HRADEK,

formance were due to a change in criteria, the False-Positive rate would increase. Third, the values of d’ increased progressively for several frequencies as a function of training. This increase in d’ was independent of the small variations in the False-Positive rate and paralleled that seen for the Performance measure for these frequencies (Fig. 5 ) . A summary of these data for all monkeys at three different S2 frequencies is illustrated in Fig. 10 by comparing the mean value of d’ over the first five sessions to the mean value of d’ over the final five sessions. This analysis is shown for S2 frequencies of 26 Hz (top), 24 Hz (middle), and 22 Hz (bottom). The increase in the measure of d’ with training provides further evidence that the improvement in performance resulted from a true increase in their frequency discrimination acuity. In contrast to these animals, by this criteria case E4 did not show an improvement in performance with training (see Figs. 2 and 8 and Table 1). This animal was also required to maintain a False-Positive rate below 15%, and, although the values were generally higher than other monkeys, they still did not vary over a wider range (Fig. 9). On the other hand, the d’ values calculated for animal E4 did not increase over the training period as was seen in the other cases but remained roughly constant across sessions (Fig. 10). Consistent with this finding, the performance functions of this animal did not steepen with training (Figs. 4 and 8A). Although some minor improvement could be demonstrated for discrimination of 20 versus 26 Hz, that improvement was not reflected by changes in the d’ values as was seen for the other animals. This evidence supports the conclusion that frequency discrimination acuity did not improve in animal E4. To test if the low-threshold values that occasionally occurred in animal E4 were attributable to a genuine performance improvement or to a reflection of criteria changes that occurred between sessions, we performed regression analysis between the uncorrected threshold measured on a given session with the False-Positive rate of that session. In well-trained animals this correlation was very low ( Y< 0.05; P > 0.1). For animal E4 there was a suggestion that the thresholds were improved in sessions in which the FalsePositive rate was high. Nonetheless, the slope of the best-fit line was very near zero (y = -0.003x + 0.074), and the correlation between these two parameters in this animal was not statistically significant ( Y = 0.30; P = 0.0 11) . As a final test, the same analysis was conducted between the False-Positive rate and the Hit rate at each presented frequency. In every case there was no correlation between these two parameters for any tested frequency for welltrained animals (Y < 0.10; P > 0.10). In monkey E4 there was a correlation between the False-Positive rate and the performance at 26 Hz, which was very near threshold for this animal. The results of this analysis for 26 Hz are shown in Fig. 11 for the animal in which performance did not improve and from a representative animal in which performance did improve (E4 and E3, top and bottom, respectively ). As stated above, the correlation was essentially zero for the well-trained animal (Y = 0.002; P = 0.983). By contrast, for animal E4, the sessions in which the performance was best at 26 Hz were also the sessions in which the False-

AND M. M. MERZENICH Increases

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Positive rate was highest (r = 0.52; P < 0.0001). These results show that, for the well-trained animal, changes in criteria cannot account for the improvements in performance at any frequency, and thus in the derived thresholds. For animal E4, the correlation of False-Positive rate and the performance, as well as the lack of any change in the


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measure of d’, indicate that this animal did not improve in performance with training, and that the recorded modest improvements could be attributed, in part, to changes in criteria.

IN OWL MONKEYS

1025

data in all other bins. Thus, even though the stimulus in bin six was always the S2, none of these animals used this timing information to obtain a reward. It is concluded from these three lines of evidence that the animals were not using simple stimulus presentation timing cues to obtain rewards. To ensure that the performance was not affected by small variations in intensity, we periodically increased the-amplitudes of the sinusoidal stimuli presented during a session. One such control of this class is presented in Fig. 12. The performance functions at the normal peak-to-peak displacement of 300 pm are shown superimposed with one having 600-pm displacement in this representative example. This difference in stimulus amplitude was perceived as a robust difference in intensity to a human observer. Performance functions and the calculated thresholds were virtually identical when stimuli of different intensity were applied. This independence of stimulus amplitude on behavioral performance, tested over a substantial amplitude range around that used in the training, was observed in all studied monkeys. On the basis of these control experiments, we concluded that intensity effects in this behavioral apparatus and paradigm were negligible. A second concern was the animal’s potential ability to move the stimulus probe to a slight degree during the trial. It was noticed on session 30 that animal El could move the stimulus probe to contact the hand mold directly on some trials. This could have resulted in the vibration of the entire mold, effectively stimulating a much greater region of skin. Subsequently, care was taken to ensure that the probe could not be moved to contact the mold during training sessions. Visual monitoring of the hand placement behavior in all monkeys indicated that these monkeys maintained their hand in an immobile position and did not move the stimulator probes. To test the possibility that these potential vibratory cues could affect the behavioral thresholds, the stimulus probe was purposefully abutted against the mold in one or two sessions for each animal. The performance at a given frequency under these two conditions was always within 1 SD of the mean (over 3 adjacent sessions) in spite of the

Control experiments Several control experiments were performed for each animal to ensure that I) the monkey was discriminating the frequency of the tactile stimulus, and 2) only the same small region of skin was stimulated on each trial. One simple way to ensure that the animal was not using a simple timing strategy was to inspect the rate of False-Positives as a function of the number of stimulus bursts (bins) in which they occurred. If the animal was using a timing strategy, the False-Positives and Hits should cluster into one or two stimulus bins. During each session, the FalsePositive rate for each bin was continuously updated and presented. Once an animal was fully trained, the False-Positive rate was equivalent across the bin of presentation. The performance at a given frequency was also consistent regardless of the bin of presentation in all presented data. This was true even of animal E4, the performance of which did not improve with training. Finally, inspection of the data collected when the S2 stimulus was presented in bin six, which was not included in the above analysis, was equivalent to

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1026

G. RECANZONE,

W. M.

JENKINS,

G. HRADEK,

robust vibratory cue that was present with the stimulus probe abutted against the mold. DISCUSSION

The tactile discrimination performance at midrange flutter frequencies improved with training in six of seven trained animals. The final thresholds were similar to those reported in humans and macaques (Goff 1967; LaMotte et al. 1975; Mountcastle et al. 1969, 1990). These studies used a two-alternative forced-choice paradigm and required the subject to indicate which one of two successively presented stimuli were higher in frequency. In the paradigm described herein, we used a modified go/ no-go procedure in which the subject had to determine whether the presented stimulus was higher in frequency than the previously presented stimulus. The thresholds determined on any given session were reliable in the well-trained animals as indicated by the low standard deviations of the mean from three consecutive sessions in the final sessions ( < 1 Hz). These thresholds were arbitrarily defined as the S2 frequency at which a correct response occurred in 50% of the presentations, corrected for the False-Positive rate for that session. False-Positive rates < 15% did not significantly affect the measured thresholds (see Recanzone et al. 199 1). This 50% measure was consistent with reports of other primates, as stated above. A second method of analysis used was the method of signal detection. This method also demonstrated a discriminable difference or “threshold” near 22 Hz for all well-trained monkeys, whereas the d’ for greater frequency differences were much larger. The temporal order of stimulus presentation in this paradigm was shorter than those using a two-alternative forcedchoice procedure, in which the stimulus durations and intervals were 1 s (Goff 1967; LaMotte and Mountcastle 1975; Mountcastle et al. 1969, 1990). This temporal order was selected because it provided many stimulus cycles per stimulus ( 13 pulses at 20 Hz), yet it was well below the duration for adaptation of peripheral inputs (Talbot et al. 1968 ) . These short-duration sinusoidal stimuli and pauses also limited the duration of the longest trials to -8 s. It is not clear how changing the timing of the stimulus presentation would affect this behavioral performance. Tactile frequency discrimination tasks are potentially contaminated by perceptual changes in the intensity of the stimulus with increasing frequency. Significant differences in the “subjective intensities” of constant-displacement sinusoidal stimuli have been described over a wide range of frequency (Goff 1967; LaMotte and Mountcastle 1975; see also Franzen 1969; Stevens 1959; Talbot et al. 1968). The difference in frequency that results in a difference in subjective intensity that is equivalent to the amplitude discrimination performance near 20 Hz in the human has been reported to be ;2-3 Hz. This implies that a frequency discrimination of a 20.Hz standard can be done with the use of subjective intensity cues for S2 stimuli of 23-24 Hz. Subjective intensity differences are believed to result from an increase in the neuronal responses to a higher frequency, because there are more stimulus cycles for any

AND

M.

M.

MERZENICH

given unit of time (von Bekesy 1959; Mountcastle et al. 1969). We were interested in defining the psychophysical performance of these animals at a task on the basis of one stimulus parameter, frequency, and then defining the neural representation of that stimulus to begin to elucidate the neural mechanism underlying this perceptual decision. If these animals used subjective intensity cues to discriminate frequency differences, a reflection of that strategy might be apparent in neuronal responses. Reliability

of psychophysical procedure

All psychophysical studies must confirm that the subject is performing the necessary perceptual task on the basis of the specific stimulus parameters of interest. Several catch trials of different classes were run on each animal to ensure that only the frequency of the stimulus provided cues to the availability of reward (see also Recanzone et al. 199 1). Catch trials in which the S2 frequency was the same as the comparison frequency or in which the tactile probe was not allowed to contact the skin eliminated the possibility that contaminating artifactual cues were generated simultaneously with the S2. In addition, no sources of cues other than the stimulus frequency were discovered by human observers specifically instructed to investigate this possibility. The possibility that the animals were using stimulus presentation timing cues can be eliminated, because the monkey’s Hit rate for a given S2 stimulus and the False-Positive rate was constant across stimulus bins. The possibility that these animals were using a simple shift in criteria to improve performance is similarly unlikely. The False-Positive rate was not allowed to increase above 15% for any animal, and the performance and d’ measure at a given frequency for each well-trained monkey was not correlated with the False-Positive rate. We conclude that the performance functions generated by these trained monkeys reflect the perceptual acuity of these animals in the tactile frequency discrimination task. Improvement

in peyformance

There was a significant, progressive improvement in performance over time in six of the seven studied animals. Early in training, there was a general improvement in performance for all frequencies resulting in a rightward shift of the psychometric functions. In the second phase, there was a successive improvement in the performance at progressively lower S2 frequencies, with the frequencies nearest to the comparison frequency improving the slowest. The two rates of improvement are demonstrated by comparing the measure of threshold taken at three different periods of training. The largest improvement occurred initially, followed by a smaller, yet still significant, improvement in the latter half of the training period. The difference in threshold between the middle and final training sessions averaged approximately one-half of the difference between the initial and middle training sessions (see Table 1). A better indication of the rate of improvement is given by the plots of threshold as a function of the days of training. These functions were much steeper in the initial stages of training as opposed to the later stages. The overall shape of


TACTILE

FREQUENCY

DISCRIMINATION

these learning curves were very similar to those described in human subjects performing a variety of perceptual-motor tasks (e.g., Neisser et al. 1963; Seibel 1963; Seminara 1960; Snoddy 1926; see Crossman 1959; Chase 1986) and can be roughly described by a power function (e.g., De Jong 1957; Crossman 1959; see Chase 1986). The definition of thresholds on adjacent, untrained digits provide evidence that the initial component of the improvement in performance with training was transferred to the adjacent, untrained digit. The initial thresholds of the adjacent digit were more similar to the thresholds on the trained digit taken over the middle portion of the training period than they were to the trained digit thresholds taken at the initial portion of the training period. Improvements in performance at other sensorimotor or “cognitive” (i.e., chess playing) tasks has been speculated to be the result of an improvement in the strategy used in solving the task by a method of selection (Crossman 1959; De Jong 1957), or by increasing the necessary memory components of the task (Chase and Simon 1973; Rayner 1958). These processes of improvement are thought to be easily transferred to other sensory surfaces and to other similar tasks (see Anderson 1980; Singley and Anderson 1989). The paradigm used in this study has a relatively simple cognitive component, because the subject was only required to discriminate along one parameter% dimension of these simple stimuli. The initial stage of improvements can be mainly attributed to the animal developing an effective strategy and generalizing it’s behavior to include all S2 frequencies, and to maximize its “vigilance” or “internal reference” to achieve this comparison. The possibility that the continued improvement in performance even after long periods of practice results from changes in the discriminability of the appropriate stimuli has been suggested (e.g., see Fitts 1964) and may better explain the more gradual improvements that occurred in the latter half of the training period. The second stage of improvement was marked by a successive improvement at each frequency and occurred at a much slower rate. This period of training also showed an increase in the slope of the psychometric function near threshold. The thresholds measured on the adjacent digit over this period did not improve at the same rate, leading to the much larger difference between the trained and adjacent digits by the final training sessions. Enough data to address this issue was only obtained in three cases; in each of them, the threshold on the trained digit decreased by a greater percent over the final sessions of training than did the threshold on the untrained digit. These differences in threshold cannot be easily explained by differences in the strategy or memory aspects of the task as the performance on the trained digit was better on the session both before and after the session on the adjacent digit. These data are consistent with the hypothesis that the second stage of improvement was the result of a noncognitive, neural or structural change that conferred some increase in discriminability on the trained skin. Transferences of improved acuity have been described previously and appear to decrease with increasing distance from the trained surface (Craig 1988; James 1890; Volkmann 1858). A few studies have also suggested that the

IN

OWL

MONKEYS

1027

overall tactile experience of an individual subject can result in an increased performance at a novel task (Davidson 1974; Craig 1988; Gisquet-Verrier and Alexinsky 1990; but see Lechelt 1988; Carlson 1989). If the “neural” component of the improvement was relatively restricted to the trained skin, one would predict that the performance at skin locations far removed from the trained site would not show a significant late component of improvement, as is suggested by the data presented here. Unfortunately, the threshold of skin surfaces far removed from the trained digit were not tested in these animals. An important observation in support of this hypothesis was that the discrimination thresholds did improve with successive training on the adjacent digit in the single case studied (E6). In this animal, thresholds were derived on digit 3 for several weeks of training, and then the training on this digit was stopped and continued on the previously untrained, adjacent digit 4. The thresholds on this “new” digit were higher than those on digit 3, but the frequency discrimination thresholds on digit 4 did progressively improve after 2 1 successive training sessions. If the transference was complete on the adjacent digit and the increased threshold on the adjacent digits was just an artifact of random fluctuations or a change in motivation on that particular session, one would not expect to see the progressive improvements with time that were similar to the second stage improvement seen for all other trained digits. The finding that the thresholds on the originally trained digit increased after the 2 1 sessions without training on that digit suggests that the effects of improvement are lost with time. This demonstration argues against the notion that the improvement is primarily dependent on a strategy or memory component, because the animal was now even more experienced at the task, given the second series of training sessions. It also supports the notion that the smaller differences in performance that occur after the initial, rapid improvement are the results of dynamic changes in nervous system representations of the stimulus, which are altered to account for improvements in discrimination performance during stimulation and training of a specific skin surface, and are relaxed when that skin surface is no longer engaged in the task. The structures within the CNS that could correspond to the areas that are altered to account for the improvements in performance are a matter of speculation. The representation of a tactile stimulus is reproduced very accurately by the peripheral afferents in both space (Darian-Smith et al. 1980; Lamb 1983; Phillips and Johnson 198 1; see Johnson 1983) and time (Gardner and Palmer 1989a,b; Johnson 1974; Lamb 1983; Lamore and Keemink 1988; Mountcastle et al. 1972; Talbot et al. 1968). The fidelity of these representations is somewhat degraded at the level of SI cortex (Hyvarinen et al. 1980; Mountcastle et al. 1969, 1990; see Johnson 1983; Gardner 1988). Nonetheless, the temporal response of neurons in SI cortex are sufficient to account for the performance at a tactile frequency discrimination task (Mountcastle et al. 1969). A large body of evidence has demonstrated that the topographic representation of the body surface is alterable in primary somatosensory cortex (see Merzenich et al. 1988, 1990 for reviews).


1028

G. RECANZONE,

W. M. JENKINS,

G. HRADEK,

This area of cortex was studied in the monkeys described in this study and did in fact demonstrate significant changes in both the distributed spatial and temporal response properties of SI cortical neurons (Recanzone et al. 1992a-c). Other cortical areas that are most probably contributing to the task are within the parietal lobe. In the macaque, areas 5 and 7a are thought to also be involved in this behavior ( Mountcastle et al. 1975 ) . These higher cortical areas may also be contributing to the first stage of improvements as described above. Time

Course

of improvements

in performance

All monkeys that showed an improvement in performance had thresholds in the initial, middle, and final stages of training that were roughly equivalent, on the order of 6-7 Hz initially (variance of 2 Hz across cases, Table 1 ), 3-4 Hz at the midpoint (variance of 1 Hz), and 2-3 Hz at the final stage (variance of 0.5 Hz). This was in spite of the fact that one monkey achieved this improvement over the course of 30 days, whereas another took up to 13 1 days. Nonetheless, when the data were normalized by the total training period, there was close agreement of the progress of each of these monkeys. This observation implies that the mechanism(s) underlying these perceptual improvements are either different for the different monkeys but achieve the same ends, or more likely, that the rates at which these mechanisms operate vary among individual monkeys. No improvement

in performance for case E4 .

One notable exception to the improvement in performance was recorded in this study. Animal E4 did not show progressive improvements in performance even though it was trained over a number of sessions equivalent to those in other monkeys (see Table 1). There are at least three possible explanations why this animal’s performance did not improve. 1) The animal was not under stimulus control and therefore was not performing the task on the basis of the tactile stimulus. 2) This animal was using subjective intensity cues to perform the task throughout the training period, and this cue was not sufficient for stimulus frequencies ~25 Hz. 3) The animal did not develop the appropriate neural representation necessary for the improvement in acuity. The first possibility is unlikely, given the arguments discussed above. The psychometric functions clearly showed that this animal performed the task well at high frequencies (>28 Hz), and the False-Positive rate was maintained below 15%, as in other animals. This implies that the animal was under stimulus control for these large S2 frequencies. Criteria shifts could account for some of the improvement in performance at frequencies near threshold (see Fig. 11) but cannot entirely account for fluctuations in performance. The distinction between the animal using subjective intensity versus some other mechanism for frequency of the stimulus unfortunately cannot be differentiated by these data, because intensity difference limens at these stimulus parameters in this species are unknown. An alternative possibility, that the animal had not developed the appropriate neural representation of the tactile stimulus, is

AND M. M. MERZENICH

strongly suggested by neurophysiological data presented in following reports (see Recanzone et al. 1992b,c). In summary, these findings show that the psychophysitally measured performance of these animals progressively improved on the tactile frequency discrimination task with the stimuli presented to a constant, restricted skin region for six of the seven studied monkeys. This improvement was primarily confined to the small region of skin that was stimulated in the behavioral paradigm, although some gains were conferred to nearby skin locations. This local improvement in acuity of a restricted skin surface may plausibly be accounted for by experience-driven changes in the neural representation(s) of that skin surface. That question is addressed in the following reports (Recanzone et al. 1992a-c). The authors would like to thank T. T. Allard and R. J. Nudo for insightful comments during the development of the psychophysical procedure,, and C. E. Schreiner and R. Beitel for helpful criticisms of earlier versions of the manuscript. Funding was provided by National Institutes of Health Grants NS10414 and GM-07449, Hearing Research, and the Coleman Fund. Present address of G. H. Recanzone: Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20892. Address for reprint requests: M. M. Merzenich, U499 Box 0732, University of California, San Francisco, CA 94 143-0732. Received 6 November 1990; accepted in final form 4 December 199 1. REFERENCES ALLARD, T. T., CLARK, S. A., JENKINS, W. M., AND MERZENICH, M. M. Reorganization of somatosensory area 3b representation in adult owl monkeys following digital syndactyly. J. Neurophysiol. 66: 104% 1058, 1991. ANDERSON, J. R. Cognitive Skills and Their Acquisition. Hillsdale, NJ: Erlbaum, 1980. VON B&&Y, G. Synchronism of neural discharges and their demultiplication in pitch perception of the skin and in hearing. J. Acoust. Sot. Am. 3 1: 338-349, 1959. BUCHHALTER, J., BRONS, J., AND WOODY, C. Changes in cortical neuronal excitability after presentations of a compound auditory stimulus. Brain Res. 156: 162-167, 1978. CALFORD, M. B. AND TWEEDALE, R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature Lond. 332: 446-448, 1988. CALFORD, M. B. AND TWEEDALE, R. Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. J. Neurophysiol. 65: 178-l 87, 199 1. CARLSON, S., TANILA, H., LINNANKOSKI, I., PERTOVAARA, A., AND KEHR, A. Comparison of tactile discrimination ability of visually deprived and normal monkeys. Acta Physiol. Stand. 135: 405-4 10, 1989. CHASE, W. G. Visual information processing. In: Handbook of Perception and Human Performance. Cognitive Processes and Performance, edited by K. D. Boff, L. Kaufman, and J. P. Thomas. New York: Wiley, 1986, vol. 2, p. 28/l-28/71. CHASE, W. G. AND SIMON, H. A. Perception in chess. Cognit. Psycho/ 4: 55-81, 1973. CHUBBUCK, J. G. Small-motion biological stimulator. Appl. Phys. Lab. Tech. Digest May-June: 18-23, 1966. CLARK, S. A., ALLARD, T. T., JENKINS, W. M., AND MERZENICH, M. M. Cortical map reorganization following neurovascular island skin transfers on the hands of adult owl monkeys. Sot. Neurosci. Abstr. 12: 391, 1986. CRAIG, J. C. The role of experience in tactual pattern perception: a preliminary report. Int. J. Rehabil. Res. 11: 167-17 1, 1988. CRONHOLM, B. Phantom limbs in amputees. A study of changes in the integration of centripetal impulses with special reference to referred sensations. Acta Psychiatr. Neurol. Stand. Suppl. 72: l-3 10, 195 1.


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Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task.

Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation.

Basal forebrain dynamics during a tactile discrimination task.

Evoked unit activity in auditory cortex of monkeys performing a selective attention task.

Dual-hemisphere transcranial direct current stimulation improves performance in a tactile spatial discrimination task.

Alpha-2 adrenergic agonists decrease distractibility in aged monkeys performing the delayed response task.

Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly.

Sex differences in response to amphetamine in adult Long-Evans rats performing a delay-discounting task.

Acute aerobic exercise enhances attentional modulation of somatosensory event-related potentials during a tactile discrimination task.

Cortical projections of area 18 in owl monkeys.

Cortical projections of posterior parietal cortex in owl monkeys.

Manual asymmetry for tactile discrimination.

Numerosity discrimination of tactile stimuli.

The effect of gender on a frequency discrimination task in children.

Optogenetics in Mice Performing a Visual Discrimination Task: Measurement and Suppression of Retinal Activation and the Resulting Behavioral Artifact.

Inhibition of return in a discrimination task.

Correction: Optogenetics in Mice Performing a Visual Discrimination Task: Measurement and Suppression of Retinal Activation and the Resulting Behavioral Artifact.

Dynamic expression of the polysialyltransferase in adult rat hippocampus performing an olfactory associative task.

Frequency and intensity discrimination in Mongolian gerbils, African monkeys and humans.

Discriminability measures and time-frequency features: an application to vibrissal tactile discrimination.

Buspirone blocks the discriminative stimulus effects of apomorphine in monkeys.

Assessing Visuospatial Abilities in Healthy Aging: A Novel Visuomotor Task.

Kinesthetic discrimination after prefrontal lesions in monkeys.

Improvement of tactile roughness discrimination acuity correlates with perception of improved hand function in patients after hand surgery.