peaked repsonses should be observed 350-400 ms after CS onset ..... Dover,. New York. Scandrett J, Gormezano 1 (1980) Microprocessor control and A/D.
Biological Cybernetics
Biol. Cybern. 65, 161-169 (1991)
© Springer-Verlag 1991
Altering the synchrony of stimulus trace processes: tests of a neural-network model * J. E. Desmond and J. W. Moore Department of Psychology, University of Massachusetts, Amherst, MA 01003, USA Received January 7, 1991/Accepted April 9, 1991
Abstract. A previously described neural-network model (Desmond 1991; Desmond and Moore 1988; Moore et al. 1989) predicts that both CS-onset-evoked and CS-offsetevoked stimulus trace processes acquire associative strength during classical conditioning, and that CR waveforms can be altered by manipulating the time at which the processes are activated. In a trace conditioning paradigm, where CS offset precedes US onset, the model predicts that onset and offset traces act in synchrony to generate unimodal CR waveforms. However, if the CS duration is subsequently lengthened on CS- alone probe trials, the model predicts that onset and offset traces will asynchronously contribute to CR out- put and bimodal CRs will be generated. In a delay conditioning paradigm, in which US onset occurs prior to CS offset, the model predicts that only the onset process will gain associative strength, and hence, only unimodal CRs will occur. Using the rabbit conditioned nictitating membrane response preparation, we found experimental support for these predictions.
1 Introduction A conditioned response (CR) can be viewed as a prediction that one event will be followed by a second event. For example, in eyeblink conditioning, a neutral tone conditional stimulus (CS) is repeatedly followed by a puff of air or mild periocular electrostimulation (the unconditional stimulus, or US). Eventually, conditioned eyeblinks that precede the US occur when the CS is presented. The prediction represented by the CR is specific in two respects. First, the CR is localized to the relevant response system, i.e., the subject blinks to the CS but does not salivate or exhibit leg flexion. The prediction is also temporally specific, a quality that can most easily be observed in a trained subject by with-
* This research was supported by National Science Foundation grant BNS 88-10624 and Air Force Office of Scientific Research grant 89-0391
holding the US and presenting a CS-alone probe trial. On such trials the CR is seen to reach its maximum at the time the US would be expected. Although the procedures for establishing CRs are often relatively simple, many variations of the basic paradigm can be achieved by manipulating the number of events that are presented during a trial, the number of different trial types, the probabilities and conditional probabilities of the events, or the timing of the events. The phenomena observed from variations such as Kamin's blocking paradigm (Kamin 1968), conditioned inhibition, or trace conditioning, for example, offer clues as to how associations among events are formed (e.g., see Dickinson and Mackintosh 1978). Temporal properties of CRs reveal additional clues (see Gormezano et al. 1983). For example, the CR anticipates the occurrence of the US, but CR onset tends to be delayed by an amount of time appropriate to the expected time of the US (e.g., Kimmel 1965). The length of the delay of the CR depends upon the CS-US interstimulus interval (or IST, defined as the interval between CS onset and US onset). The CR reaches its peak magnitude at the time the US occurs (e.g., Cole- man and Gormezano 1971; Smith 1968), but the CR timing is also adaptive in that changing the CS-US interval produces a corresponding change in the time of peak (Coleman and Gormezano 1971). Double peaks are also observed if the CS-US interval alternates between two different values (Hoehier and Leonard 1976; Millenson et al. 1977). We have previously presented a model of conditioning that simulates the timing characteristics of CRs described above. Details of the model are given in recent articles (Desmond 1991; Desmond and Moore 1988; Moore et al. 1989). The network architecture is illustrated in Fig. 1. Basically, each CS is assumed to activate two tapped delay-lines: One at the onset of the CS and another at the offset. These tapped delay-lines represent one possible realization of hypothesized stimulus trace processes, which have had an important role in learning theory (Anderson 1959; Gormezano 1972; Gormezano and Kehoe 1981; Gormezano et al. 1983;
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Fig. 1. Diagram of the network. CS onset and CS offset are assumed to activate separate tapped delay-line stimulus traces. The taps form modifiable connections - denoted by closed (- !) synaptic terminals with the V and E units. The CR is generated when V-unit connections that have positive weights are activated. Modified from Desmond and Moore, 1988. Copyright 1988, Springer-Veriag
Guthrie 1933; Hull 1943; Kamin 1965; Patterson 1970; Pavlov 1927). Each tap forms a modifiable connection with two units, labelled V and E (modifiable connections appear as triangles in Fig. 1). The amount of change in connection strength (also referred to as connection weight) that is possible for a tap is maximum when the delay line element is initially activated. The eligibility for modification (Klopf 1986, 1988; Sutton and Barto 1981) decreases rapidly for E-unit connections and less rapidly for V-unit connections. In addition to synaptic eligibility, changes in E-unit connections also depend on the CS-US ISI and on the discrepancy between a teaching signal (the US) and the output of the E-unit. Changes in V-unit connections similarly depend on synaptic eligibility and the CS-US ISI; in addition, changes in these conditions depend on the output of the E-unit, and on the discrepancy between the teaching signal and the output of the Vunit. The function of the E-unit is to learn the time that a US occurs relative to the onset and offset of all CSs. With repeated CS-US presentations, the E-unit starts sending a signal to the Vunit when a US is expected. This signal permits V-unit connection strengths to be modified. The network's output (the simulated CR) is derived from the V-unit. As each tap is activated, its connection weight contributes to the magnitude of the CR, affecting it in either an excitatory (positive weight) or inhibitory (negative weight) manner.
The ability of the model to predict uni- and bimodal CR waveforms was demonstrated by a simulation of Millenson et al.'s (1977) experiment. In this experiment, a tone CS was presented at a short CS-US ISI on some trials, and at a long interval on the other trials. On long CS-alone probe trials, double-peaked CRs were observed, with each peak occurring at its corresponding CSUS ISI. Single-peaked CRs were observed on short CS-alone trials, and this peak occurred at the short CS-US ISI. The model simulates these results because two sets of positive V-unit connections develop for the onset taps. These two sets generate double-peaked responses on long CS trials. On short CS trials, the second onset peak is suppressed by inhibitory V-unit connections that develop for the offset taps (see Figs. 7-10 in Desmond and Moore 1988). Thus, the model's explanation for Millenson et al.'s (1977) results relies on the assumptions that (a) connections of onset and offset taps develop independently, and (b) the relative timing of onset and offset connections can be manipulated, i.e., onset and offset connections can be made to influence the CR output at the same time, or at different times, by altering the duration of the CS. These assumptions are particularly important in simulating trace conditioning, a protocol in which the onset of the US occurs after the offset of the CS. The interval between the offset of the CS and the onset of the US is referred to as the trace interval. The left side of Fig. 2 shows that during trace conditioning training, the network develops excitatory onset and offset connections. Each connection is depicted as a solid vertical bar, and the height of the bar represents the strength of the connection. Time is represented along the X-axis, and each connection is represented at the time of its activation. By increasing the duration of the CS, depicted on the right side of the figure, the timing of the onset and offset elements is shifted. The model makes the novel prediction1 that increasing the CS duration should produce double-peaked CRs. The first peak should occur at the CS-US ISI; the second peak should occur after the offset of the CS, by an amount of time equal to the trace interval. The figure also illustrates that the individual peaks of the double-peaked response should be smaller in magnitude than the amplitude of the single-peaked response. This prediction results from the assumption that the amplitude of the CR at any given time is proportional to the sum of the connections that are active. This sum can be maximized only if the onset and offset connections are concurrently activated. The model predicts that if the trace interval is zero ms in duration, the offset connections will not gain strength. In classical conditioning terminology, a zero ms trace interval constitutes a delay conditioning protocol. Figure 3 illustrates that, because only the onset taps develop excitatory strength, changing the CS duration should not affect the timing or amplitude of the CR.
1
This prediction was described in Desmond and Moore 1988 (see Fig. 6)
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Fig. 2. The temporal distribution of onset and offset weights in trace conditioning, and a prediction of CR topography when the timing of onset and offset processes is shifted. Each hash mark along the Xaxes represents 10 time steps. Left: When a trace conditioning protocol is simulated, both onset and offset weights develop excitatory strength. The unirnodal CR that results is generated by the summation of the two sets of weights. Right: If, after trace conditioning training, the duration of the CS is extended, the onset and offset weights contribute to the CR at different times and a bimodal CR is predicted. Modified from Desmond and Moore (1988). Copyright 1988, Springer-Verlag
Fig. 3. The temporal distribution of onset weights in delay conditioning. Each hash mark along the Xaxes represents 10 time steps. Left: In delay conditioning, the model predicts that only onset connections develop excitatory strength. Right: The model predicts that changing the duration of the CS after delay conditioning should not affect the timing or amplitude of the CR
In the present paper, we describe a test of these predictions, using the rabbit conditioned nictitating membrane response preparation2. In a Trace Group, we first trained rabbits using a trace conditioning protocol. The CS-US ISI was 350 ms, the CS duration was 150 ms, the US duration was 50 ms, and the trace interval was 200 ms. After this initial training, trace conditioning trials interspersed with CS-alone probe trials were presented. For the probe trials, three different CS durations were presented:
A Delay Group was also trained. In this group, the CS duration was 350 ms, the CS-US ISI was 350 ms, and the trace interval was zero ms in duration. The model predicts that onset, but not offset, connections will gain strength, and that singlepeaked repsonses should be observed 350-400 ms after CS onset on all three probe trial types.
2 Methods ! 150 ms duration. The model predicts that onset and offset weights will be concurrently activated, so a single peak at 350400 ms after CS onset is predicted. ! 400 ms duration. The model predicts a peak at 350- 400 ms, and a second peak at 600-650 ms. ! 600 ms duration. The model predicts a peak at 350- 400 ms, and a second peak at 800-850 ms. 2
The defensive eyeblink reflex of the rabbit consists of eyeball retraction, extension of the nictitating membrane across the cornea, and closure of the eyelids. The nictitating membrane response has been the traditional measurement in conditioning literature ever since Gormezano's (1966) description of the preparation. However, nicititating membrane movement is closely coupled with orbicularis oculi and extraocular muscle activity (Berthier and Moore 1990)
2.1 Subjects A total of 16 New Zealand albino rabbits (8 Trace, 8 Delay) weighing approximately 2.0 kg served as sub- jects for this experiment. The rabbits were housed indi- vidually and had free access to food and water. 2.2 Apparatus The conditioning apparatus and procedure for recording NM movement have been described by Gormezano (1966). Basically, rabbits were restrained in Plexiglas boxes and conditioned in ventilated and fireproofed file drawers. The US was electrostimulation administered
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via stainless steel wound clips, one of which was attached just below the eye, the other just posterior to the eye. The US consisted of a 50-ms train of 2.5-ms DC monopolar pulses having a 12-ms interpulse interval. The US magnitude was 1.0 mA. The CS consisted of an 80-dB (SPL) 1200-Hz tone that was presented via a speaker mounted directly in front of the rabbit's head. CRs and URs were recorded using a photoelectric transducer (Gormezano and Gibbs 1988) that was affixed to a removable headmount. A small loop of Ethilon 6-0 nylon that was sutured to the NM was attached to the transducer's arm. The arm consisted of an L-shaped piece of tubing, and rotary movements of the arm produced voltage changes in the transducer. The timing of stimulus events and A/D conversion of the NM movement was controlled by an Apple IIe computer. The interfacing and software employed were developed by Scandrett and Gormezano (1980). NM movement was sampled at 100 Hz. For each trial, 2.5 s of data were digitized, including a 200-ms pre-CS period. The data were stored on floppy disks and later transferred to a Sun 3 workstation for subsequent analyses.
difference was not statistically significant (tl4 =1.285, p > 0.05). Similarly, on the first day of Phase 2, the percent CRs occurring on reinforced trace trials for the Trace Group (80.6%) was not significantly different from the percent CRs observed on reinforced delay trials for the Delay Group (72.1%) (tl4= 0.685, p > 0.05). The lack of difference between trace and delay conditioning at a 350-ms CS-US ISI is consistent with previously published reports (see Gormezano et al. 1983).
3.1 CR waveforms Figure 4 illustrates the averaged CR topographies observed in Phase 2. Waveforms for the Trace Group are in the left column, and waveforms for the Delay Group are in the right. Time is represented along the X-axis and amplitude (in mm increments) is represented on the Y-axis. The trial type for each waveform appears in the upper left corner of the panel. The horizontal trace below each waveform depicts the onset and offset of the CS. For the reinforced Training trials, a US marker appears below the CS marker. The thickness of the CR waveform at any given time reflects ± 2.0 standard errors of the mean amplitude. The dotted vertical lines appear at 100-ms intervals.
2.3 Procedure Each rabbit received two days of initial preparation prior to training. On the first day, the loop of suture was attached to the NM and the rabbit was allowed to sit in the conditioning apparatus for 30 min with the transducer mounted on the head. On the second day, the rabbit was again placed in the conditioning apparatus for 30 min and the transducer was mounted on the head. In addition, the arm of the transducer was attached to NM's suture and the US leads were attached. Neither the CS nor the US was presented on the two preparation days. All rabbits received two phases of training. The first phase consisted of 2-3 days of acquisition training using a CS-US interval of 350 ms. The Trace Group received trace conditioning trials with a 150-ms CS duration and 200-ms trace interval. The Delay Group received delay conditioning in which the onset of the US began at the offset of the 350-ms CS. Training for Phase I and Phase 2 consisted of 100 trials per day at a mean intertrial interval of 20 s. Phase 2 training, which was conducted for 5 days, consisted of 85 Phase I trials plus 15 probe trials per day. The probe trials were of three different types (5 each), PI 50, P400, P600, and consisted of nonreinforced presentations of the CS at durations of 150, 400, or 600 ms, respectively. The probe trials and their sequence of presentation were identical for the Trace and Delay Groups.
3 Results The percentage of CRs observed at the end of Phase I training appeared to be slightly greater in the Trace Group (63%) than in the Delay Group (43%), but the
Fig. 4. CR waveforms for 8 Trace Group and 8 Delay Group rabbits averaged over 5 days of Phase 2 training. The trial types designated "Training" were presented on 85% of the trials, whereas each of the probe trials, P150, P400, and P600, were presented on 5% of the trials
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The expected time of the US relative to the onset or offset of the CS, as predicted by the model, is depicted by a set of solid vertical lines in Fig. 4. For the Delay Group, the model predicts a single US expectation and a single CR peak at 350-400 ms after CS onset. For the Trace Group, the model predicts US expectations and peaks at 350-400 ms after the onset of the CS and 200-250 ms after the offset of the CS. For the P150 probe, these two expectations temporally coincide. However for the P400 and P600 probes these expectations are temporally displaced, and this displacement is illustrated by the two sets of vertical lines. The averaged CR topographies depicted in Fig. 4 are consistent with the -model's predictions. Single- peaked waveforms were observed for all probe types in the Delay Group and for P150 in the Trace Group. Double-peaked waveforms were observed for P400 and P600 probe trials in the Trace Group, with peaks occurring near the predicted times. To statistically test for differences in the probe trial topographies, each trial was divided into four time zones: (a) 550650ms, (b) 680-780ms, (c) 800- 900 ms, and (d) 1000- 1100 ms. The average amplitude within each time zone was computed, and these amplitudes were subjected to an analysis of variance with Group (Trace vs. Delay) as the between subjects factor and the following within-subjects factors: Probe trial type (3 levels), Repetitions (5 presentations of each probe trial per day), Days (5 days of Probe 2 training), and Time Zone (four zones as described above). The main finding of this analysis was a significant Group x Probe x Time Zone interaction (F6,84 = 36.7, p < 0.001). That is, CR topographies depended on both type of probe trial and group. Trend analyses3
3
Orthogonal trend comparisons were conducted on the Time Zone variable. The time zone intervals were not equally spaced, so orthogonal coefficients were generated as suggested by Keppel (1973, pp. 581-589). Significant curvilinear trends (i.e., both linear and quadratic trends significant) were found in the Delay Group for both P150 (F1,7linear = 11.2, p < 0.025; F1,7quadratic = 11.5, p < 0.025) and P400 (F1,7linear = 108.7, p < 0.001; F1,7quadratic = 10.8, p < 0.025), and for P150 for the Trace Group (F1,7linear = 60.8, p < 0.001; F1,7quadratic = 20.1, p < 0.01). P600 of the Delay Group showed a significant linear trend only (F1,7linear = 11.2, p < 0.025). P400 of the Trace Group had significant linear and cubic trends (F1,7linear = 8.5, p < 0.025; F1,7cubic = 24.8, p < 0.001), whereas P600 of the Trace Group had a significant quadratic trend only (F1,7quadratic = 20.3, p < 0.01) A significant Group x Probe x Time Zone x Repetitions effect was also found (F24,336 = 1.618, p < 0.05). Analysis of trend components across the five levels of repetitions revealed some subtle effects, e.g., P400 of the Trace Group had significant linear and cubic trends on the first two repetitions, but only significant cubic trends on the last three repetitions. However, we determined that these analyses did not significantly change the overall conclusions reported above. The Group x Probe x Time Zone x Days interaction was not significant, indicating that the differences in waveforms between Trace and Delay subjects for the different probe trials did not appear to change over days.
indicated that (a) The CR waveform for the Delay Group's P400 probe was similar to the CR waveform of the Trace Group's P150 probe. The model predicts that unimodal CRs should be generated for both probe types, and thus, the observed trend similarities are consistent with the model. (b) The bimodal CR waveform for the Trace Group's P400 probe was different from that of the Trace Group's P600 probe. For the Trace Group the model predicts that, as CS duration is increased, temporal separation between first and second peaks should also increase. Thus, the observed differences in trend between P400 and P600 of the Trace Group are also consistent with the model's predictions. 3.2 Analysis of peaks Examination of individual trials were revealed that the two peaks observed in the averaged topographies for P400 and P600 of the Trace Group were not derived exclusively from double-peaked CRs. Single-peaked CRs, with the time of peak alternating between two times, were also observed. In order to separate these different peak types, we developed analysis routines designed to find the amplitude and time of all local CR peaks for each trial4. Trials were classified by the number of peaks and by the time that peaks occurred. For all probe trials in both Trace and Delay Groups, if a peak occurred 150-500ms after CS onset it was considered an early peak. For all probe trials except P600 of the Trace Group, a peak occurring greater than 500 ms after CS onset but less than or equal to 950 ms after CS onset was considered a late peak. For P600 of the Trace Group, a late peak was defined to be greater than 700 ms after CS onset but less than or equal to 950 ms after CS onset. Each trial was classified as having either (a) zero peaks, (b) a single early peak, (c) a single late peak, or (d) two peaks (a double peak). To be considered a double-peaked trial, one early and one late peak had to be present. Nearly all of the trials observed fell into one of these four categories. Of the 1200 probe trials for both the Trace and Delay Groups, only 23 trials (1.9%) did not fit into one of the above four classifications, and were not subjected to subsequent analyses of amplitude or latency. An additional 20 trials (1.7%) were discarded because movement occurred during the 200-ms pre-CS baseline period. For both the Delay and Trace Group, single-early peaks were observed most often. However, for P400 and P600 of the Trace Group, but not for P150 of the Trace Group, nor for any probe type in the Delay Group, a statistically significant number of double-
4
A local peak was defined to occur at time t if (a) the CR amplitude was the maximum in the window 150 ms before to 150 ms after t and (b) the CR amplitude at t was at least 0.25 mm greater than the smallest amplitude 0-150 ms before t and 0- 150 ms after t
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Fig. 5. Averaged CR waveforms of single-early, single-late, and doublepeaked CRs for P400 and P600 probe trials of the Trace Group
peaked trials was observed5 (χ12 = 4.34, p < 0.05 for P400; χ12 = 10.64, p < 0.01 for P600). In addition, for the Trace Group, P400 probes exhibited significantly more single-peaked CRs and fewer double-peaked CRs than P600 probes (χ12 = 4.23, p < 0.05). Figure 5 illustrates for P400 and P600 of the Trace Group, the averaged CR topographies of those trials that were classified as having single-early, single-late, or double-peaked responses. All three of these response-types were observed in 5 of the 8 Trace subjects. Of the remaining three Trace subjects, one subject made single-early and single-late peaks and a large number of no responses, but no double peaks. The second subject made singleearly and double peaks but almost no single-late peaks, and the third almost always made single-early peaks.
averaged over the 5 days of Phase 2. The mean ±1.0 S.E. of these averages are depicted in the lower portion of Fig. 6. For the 8 Delay Group subjects, single-early peak amplitudes were averaged over 5 days for PI 50, P400, and P600, and the mean ±1.0 S.E. of these averages appear in the top portion of Fig. 6. Peak amplitudes for P150 of the Trace Group did not significantly differ from P400 of the Delay Group (t11 = 0.97, p > 0.05). Thus, there did not appear to be an overall difference between trace and delay conditioning as assessed by peak amplitudes of the relevant probe trials. A repeated-measures analysis of variance for the Delay Group revealed a significant effect of peak type (F2,14 = 9.146, p < 0.003). Subsequent t-tests indicated that peak amplitudes for P150 were significantly smaller than those for either P400 (t14 = 3.87, p < 0.01) or P600 (t14 = 3.5l, p < 0.01). A repeated-measures analysis of variance of the Trace peak amplitudes also revealed a significant effect of peak types (F8,32 = 2.625, p < 0.025). A least significant difference (Keppel, 1973, p.135) was computed to compare peak types. Referring to Fig. 6, note that peak amplitudes fall into one of the three ranges: less than 2.0 mm, about 2.4 mm, and 3.0 mm or greater. Peaks in the first and third ranges were found to be significantly different from each other. Differences between amplitudes in the first and second ranges, or in the second and third ranges, were not significant. These analysis indicate that, in partial support of the model's prediction, the first peak of a double-peaked response had a significantly smaller amplitude than that of the unimodal CR observed for P150. The second peak of the double, however, was not significantly different in amplitude from the P150 peak. For P400, the second peak of the double was significantly larger in amplitude than the first, but the two peaks were not significantly different from each other for P600. We address these findings and their implications for the model in the Discussion.
3.2.1 Peak amplitudes. It is evident from Figs. 4 and 5 that there are 9 different types of peaks to compare for the Trace Group. These types are: single-early peaks for P150, P400, and P600, single-late peaks for P400 and P600, the first peak of a double peak for P400 and P600, and the second peak of a double for P400 and P600. For the 5 Trace subjects that displayed singleearly, single-late, and double-peaked responses, peak amplitudes for each of the 9 different peak types were
5
To test the null hypothesis that subjects made only single-peaked CRs we let nE, be the total number of early peaks, and nL be the total number of late peaks. The probability of an early peak, pE is nE / (nE + nL), and the probability of a late peak, pL is nL / (nE + nL). Let N be the total number of trials. Under the null hypothesis, the expected number of trials containing an early peak is equal to (N)(pE), and the expected number of trials containing a late peak is equal to (N)(pL)
Fig. 6. Mean amplitude ( ±1.0 S.E.) of CR peak for each of the different types of peaks observed for the Trace and Delay Groups. Amplitude in mm is depicted on the X-axis
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Fig. 7. Distribution of latencies of CR peaks for P150, P400, and P600 probes for the Trace and Delay Groups. For each graph, time (in ms) from onset of the CS is depicted along the X-axis, and the number of
peaks is depicted on the Y-axis. The height of a striped bar represents the total number of peaks (single- plus double-peaked CRs). The height of a solid bar represents the number of peaks from double-peaked cases
3.2.2 Peak latencies. Figure 7 illustrates for both the Trace and Delay Groups the distributions of latencies of CR peaks for each probe trial type. For each panel, time (in ms) from CS onset is depicted along the X-axis, and the number of peaks observed at a particular time is depicted on the Y-axis. The height of a solid black bar represents the number of double-peaked CRs. The height of a striped bar represents the total number of peaks, including double-peaked CRs. (As an example, the figure indicates that a total of 8 CR peaks occurred at 800 ms for P600 of the Trace Group. Three of these were from double-peaked CRs, and 5 were from single-peaked CRs). The figure represents peaks from 8 Trace and 8 Delay rabbits, and the only trials that were excluded were those that contained movement
during the 200-ms pre-CS baseline period (20 trials) and those that had more than two peaks (4 trials). Note that for P400 and P600 of the Trace Group, a separate distribution of latencies appears to be clustered around each time of US expectation. Figure 8 summarizes latencies of peaks for the different peak types for the Delay Group (N = 8) and for the 5 Trace rabbits that exhibited single-early, single-late, and double-peaked CRs. Mean ± 1.0 S.E. are depicted. The leftmost pair of dotted vertical lines represents the onset and offset, respectively, of the US with respect to the onset of the CS. The middle pair of dotted vertical lines represents the onset and offset of the US with respect to the offset of the P400 probe. The rightmost pair of dotted vertical lines represents the
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Fig. 8. Mean time of CR peak ( ± 1.0 S.E.) for each of the different peak types of the Trace and Delay Groups. Time is depicted along the X-axis
onset and offset of the US with respect to the offset of the P600 probe. The mean peak latency for P150 of the Trace Group did not differ significantly from P400 of the Delay Group (t11 = 0.11, p > 0.05). A repeated-measures analysis of variance performed on peak latencies of the Delay Group revealed a significant effect of peak type (F2,14 = 21.8, p < 0.001). Subsequent t-tests indicated that peak latency for P150 was significantly less than that of P400 (t14 = 5.68, p < 0.001) and P600 (tl4 = 5.75, p < 0.001). For the Trace Group, the analysis of variance of peak times also yielded significant differences among the groups (F8,32 = 211.6, p < 0.001). However, because the groups were formed partly on the basis of peak time, the only relevant comparisons are among the early or among the late peak types. For the early peak types, t-tests revealed that the first peak of the double from P400 was the only early peak type that differed significantly from P150 (t32 = 3.37, p < 0.01). The difference between single-late and double-late peak latencies was not significant for either P400 or P600.
4 Discussion The results of this experiment are consistent with the prediction described in Desmond and Moore (1988): CR peaks were observed at two different points in time when the duration of a traceconditioned CS was lengthened. The first peak occurred at the CS onset-US interval (350 ms), and the second peak occurred 200 ms after CS offset. These timing relationships were observed for both P400 and P600 probe trials, and thus, it is not likely that second peaks were nonspecific blinks evoked by the novelty of the lengthened CS. An interesting aspect of the results was the occurrence of single-early, single-late, and double-peaked responses observed in P400 and P600 of the Trace Group. The model predicts that only double-peaked CRs should occur on these probe trials. To account for these response types within the framework of the model, we offer the following hypotheses. (a) Synaptic weights produce a CR when the sum of the active
weights exceeds a threshold. This threshold fluctuates from trial to trial. (b) The output from the V-unit is "refractory", i.e., a new CR cannot occur until the sum of the active weights once again falls below threshold. (c) Activation of weights causes a rapid but transient decrease in threshold. The threshold increases when activation ceases6. These threshold hypotheses can account for single-early, single-late, and double-peaked trial types observed for P400 and P600 of the Trace Group. Single-early peaks would occur when the threshold at the start of the trial is low. The offset weights would be activated while the response is still refractory, and thus, the second peak would not occur. Single-late peaks would occur if the threshold is initially high. The onset weights would fail to elicit a response, but would lower the threshold sufficiently so that the subsequently active offset weights could elicit a response. Double-peaked responses would occur when the threshold is at an intermediate level, i.e., sufficiently low for the onset weights to elicit the first peak, but sufficiently high so that onset weights can fall below threshold in time for the offset weights to elicit the second peak. Other aspects of our Trace Group results are also consistent with these hypotheses. For example, more double-peaked responses were observed on P600 probes than on P400 probes. To account for this, note that the time between activation of the onset and offset weights would be half as long for P400 probes (200 ms) as it would be for P600 probes (400 ms). By hypothesis (c) above, the threshold level at the time the offset weights are activated would be lower for P400 than for P600. Consequently, it would be more likely for P400 than for P600 probes that output is still refractory at the time the offset weights are activated; thus, double-peaks would be more likely on P600 probes. In support of the hypothesis that the P400 threshold is lower than the P600 threshold when the offset weights are activated, Figs. 5 and 6 reveal that late peaks on P400 probes tend to be larger in amplitude than late peaks on P600 probes. Based on this observation, we would hypothesize that the activation of onset weights produces a decrease in threshold that lasts at least 200 ms (i.e., the time separating the solid vertical bars for P400 in Fig. 5), but less than 400 ms (the time separating these bars for P600 in Fig. 5). The time lag between activation of onset weights and the decrease in threshold is difficult to estimate, but would have to be less than 200 ms. Relatively short peak latencies were observed for the first peak of the P400 double-peaked response; this can be seen in Figs. 5 and 8. These short latencies are also consistent with our threshold hypotheses. If the
6
In terms of the model presented by Desmond and Moore (1988), Y(t), the output of the system, was a smoothing function of s(t), where s(t) is the weighted sum of the tapped delay-line inputs plus the US input. To implement the above hypotheses in the model, we might have Y(s(t), θ(s(t-p), R(t))), i.e., Y would be a function of both s and a threshold, θ, which in turn is a function of prior values of s, (p denoting the time lag) as well as a slowly varying random process R(t)
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first peak occurs earlier than normal, there is more time for the threshold to rise before the offset weights are activated, and thus, a greater chance that a double-peak will occur. For the Delay Group, the model of Desmond and Moore (1988) predicts that the CR should be influenced only by the weights of the onset taps. Thus, the reduction in CR magnitude observed for the Delay Group on P150 trails (Fig. 4) is not predicted by the model. The inability to predict this result is perhaps due to the simplifying assumptions regarding the tapped delay-line activation. That is, we have assumed that the delay-line is a one-dimensional array of elements and that, once activity is initiated, propagation of activity along the delay line proceeds without-degradation. A more neurobiologically plausible mechanism has been proposed (Desmond 1991), in which there is spreading activation of stimulus trace elements. That is, the delayline is no longer a line, but rather a plane of elements. Activity propagates further into the plane over time, but also spreads laterally. With such a mechanism, a brief CS might produce less spreading activation and recruit fewer elements than a long CS. With a delay conditioning protocol, training takes place in the presence of a long CS. Thus, when a brief CS is presented, only a subset of the trained elements would be activated, resulting in a CR of reduced magnitude. In summary, whether the tapped delay-line stimulus trace is a neurobiologically plausible mechanism, or simply an analogy for the timing processes that underlie conditioning, is an open question. If it is an analogy, it is at least a useful one for generating testable hypotheses. Other models sufficient for generating CR waveforms have been proposed (Bartha et al. 1991; Grossberg and Schmajuk 1989), and may offer different insights on timing processes. The timing mechanisms assumed in these models are speculative, as is our mechanism. But speculation is almost inevitable, as current knowledge of the anatomy and physiology underlying conditioning does not easily allow for "bottom-up" approaches to modeling. The alternative "top-down" approach, perhaps also describable as "conjecture and refutation," can be productive if experimental methods can assess under what conditions the analogies break down.
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Dr. John E. Desmond Department of Psychology University of Massachusetts Amherst, MA 01003 USA
