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The effect of stimulus omission and interstimulus interval (ISI) on electrodermal habituation at short ISIs.

The precision with which people encode and store the temporal relationships between stimuli is an area of experimental psychology where there is still considerable uncertainty. This study investigates the encoding of temporal information in the context of habituation of the orienting response, a well-studied physiological response to novel stimuli, a component of which is the skin conductance response.

Theories of habituation of the orienting response can be divided into two general types, comparator theories and non-comparator theories. Comparator theories, including those of Sokolov (1963) and Wagner (1978), postulate that the elicitation of an orienting response follows the comparison of afferent stimulation with an internal trace of past stimulation. The magnitude of the orienting response is then directly related to the degree of disparity between the internal trace and afferent stimulation. Non-comparator theories, notably dual-process theory (Groves & Thompson, 1970; Thompson, Berry, Rinaldi & Berger, 1979), do not postulate a specific trace of previous stimulation but rather suggest that the behavioural outcome of repeated stimulation is the result of the interaction of the independent processes of inferred habituation and inferred sensitization within the stimulus-response pathway.

An area of debate within the study of habituation is the extent to which changes in the temporal presentation of a stimulus, such as varying the interstimulus interval (ISI) of a stimulus series or omitting a stimulus after a series has been presented, affect habituation of the orienting response. Comparator theories of habituation (Sokolov, 1963) posit that the magnitude of the orienting response is proportional to the difference between afferent stimulation and the expected stimulation predicted by an internal neuronal model of previous stimulation. While all theories of habituation are, at some level, presumably constructed of neurons, in this paper the term neuronal model refers to an internal neural trace of previous stimulation which may be compared to the afferent stimulus. Stimulus features hypothesized to be encoded by the neuronal model include temporal parameters such as the ISI of an individual stimulus series or the temporal relationships between a number of stimuli. Therefore, if a stimulus initially presented at a regular ISI is then presented at a variable or irregular ISI, there will be an increase in the magnitude and frequency of the orienting responses, and if a series of stimuli presented at a regular ISI ceases, then there will be an omission response at the time the next stimulus would have been presented.

Dual-process theory (Groves & Thompson, 1970) does not explicitly provide mechanisms by which the ISI of a stimulus series may be encoded and therefore it would predict that omission of a stimulus which had been previously presented at a constant ISI should not result in the emission of an electrodermal response. The existence or otherwise of the effect of ISI variability on the orienting response and the presence and magnitude of the response to stimulus omission depend on the presence of temporal encoding in the formation of the neuronal model and are therefore useful indicators of the validity of competing theories of habituation. The importance of time encoding extends beyond habituation into classical conditioning where the time interval between a conditioned and unconditioned stimulus appears to be encoded (Barnet, Grahame & Miller, 1993) and mechanisms of temporal encoding have been included in neural network models such as those of Buonomano & Mauk (1994) and Klopf, Morgan & Weaver (1993). Further elucidation of the precision and extent of time encoding in habituation could be used to form more accurate models of cognition.

Experimental investigations of the effect of ISI variability on habituation of the orienting response have been equivocal in their results. The studies of Schaub (1965) and Pendergrass & Kimmel (1968) provide some evidence for variable ISIs resulting in slower rates of habituation, while the data of Gatchel & Lang (1974) and Badia & Harley (1970) suggest that there is no difference in habituation rate in variable and fixed ISI conditions. Consequently both Graham (1973) and Stephenson & Siddle (1983), in reviews of the area, are reluctant to either confirm or reject the existence of this phenomenon. It is interesting to note that all of these studies use ISis of [greater than] 20 seconds. It is possible that the length of ISI employed in these studies has limited the ability of the participants to encode the temporal parameters of the stimulus series and thus led to the generally mixed results.

The studies of response to complete stimulus omission are similarly inconclusive. However, an electrodermal response to complete stimulus omission is reported in 43-80 per cent of participants (Barry, 1984; Barry & O'Gorman, 1987; O'Gorman, 1989; O'Gorman & Lloyd, 1984; Siddle & Heron, 1976). It is not clear which individual differences are linked to the production of an omission. response in individual participants, although some evidence has been found supporting the hypothesis that omission responses are more likely to be elicited in participants with higher levels of electrodermal lability (O'Gorman & Lloyd, 1984; Siddle & Heron, 1976). The studies of response to complete stimulus omission cited above used ISis of between 13 and 21 seconds, a length which may reduce the ability of the participant to encode the temporal parameter of the stimulus series presented to him or her.

The major reason for studies employing electrodermal measures to use ISis of this magnitude is the difficulty in distinguishing between the effect of interaction between the responses to current stimuli and preceding stimuli if the interval between them is small (Grings & Schell, 1969). Experimenters have therefore used reasonably long ISis in an attempt to ensure that the response to each stimulus is free of contamination from previous responses. While this is a sensible precaution, it has restricted the design of experiments on habituation of electrodermal responses. Experiments using event-related potentials (ERPs) as the dependent measure have been generally conducted with much shorter (commonly 1-2s) ISIs. Some components of the ERP share some properties with autonomic measures of the orienting response (Barry, Cocker, Anderson, Gordon & Rennie, 1992; Kenemans, Verbaten, Sjouw & Slangen, 1988; Naatanen & Lyytinen, 1989) and there is some evidence that certain ERP components may be sensitive to stimulus omission (Simson, Vaughan & Ritter, 1976). It would therefore be useful if studies using skin conductance response (SCR) as the dependent variable could be conducted at shorter ISis than was previously the case.

It is theoretically plausible that short ISis could be encoded by participants more easily, rapidly and precisely than longer ISIs. For example, if ISI was encoded by alterations in the spontaneous firing rate of a periodically firing pacemaker neuron then there could be bounds on the degree of alteration possible from the spontaneous firing rate; these bounds could enable the encoding of short ISis but not longer ISis. Alternatively, ISI could be encoded by delay or expectancy loops which were incapable of encoding ISIs longer than a certain duration. A more complete examination of temporal predictability and habituation of the orienting response would include experiments using both short and long ISis rather than the longer ISis of the previous studies.

To achieve the aim of investigating the effect of temporal predictability on habituation of autonomic indices of the orienting response at short ISis a new scoring technique was devised. The essence of the technique is that all responses occurring within an interval of a given length are scored and then the measures obtained from this interval are compared with indices scored in other intervals of equal duration. For example, in an experiment investigating the effect of a variable ISI on the orienting response at ISis of the order of 1 s, there might be a series of stimuli presented at a constant ISI which is then replaced with a series of stimuli presented at a variable ISI. With such a short ISI it is impossible to accurately relate each SCR to a particular stimulus presentation, so we define two equal length scoring windows, say the final 10 seconds of the constant ISI series and the first 10 seconds of the variable ISI series. We then compare the various SCR indices within each window to test if the change from a constant ISI to a variable ISI resulted in a significant change in SCR activity. The SCR indices measured in each scoring window employed in the current study are maximum SCR amplitude (the largest response), the total SCR activity (sum of all SCRs in the scoring window) and the number of SCRs in the window greater than 0.02 [[micro]seconds] in magnitude.

An advantage of this scoring technique when it is coupled with a repeated measures design is that the occurrence of non-specific SCRs (NSRs) should not differentially affect one condition compared to another. If NSRs occur randomly over time then they are just as likely to fall in the scoring window corresponding to any of the different conditions and tend simply to add a random, background level of activity to the SCR scores which is equal in all conditions and does not affect the differences between the conditions. In between-subjects designs, participants with different levels of electrodermal lability (number of NSRs emitted in a given interval) may be differentially assigned to conditions and either affect the testing of the effect of the independent variable, or necessitate statistical adjustment of the scores.

The current experiment tests the effects of ISI variability and complete stimulus omission on the electrodermal response with ISis in the order of 1 to 2 seconds rather than the 10 to 20 seconds of previous studies. It was also designed to test whether the administration of instructions suggesting to the participant that the stimulus series would have the properties of a clock would have an effect on temporal processing. Such contextual cueing may be predicted to have an effect on the neuronal model by a mechanism like the retrieval-generated priming of Wagner's (1978) priming theory or alternatively affect the significance attached to the series by the participant and mediate the elicitation of a response to stimulus omission (Barry & O'Gorman, 1987).

Method

Participants

Participants were 26 university student volunteers. There were 11 males and 15 females.

Apparatus

Skin conductance was recorded by applying a constant voltage of 0.5 V across domed Ag-AgCl electrodes with 0.05 M NaCl electrolyte. The electrodes were placed on masked areas on the distal phalanges of the index and second fingers of the participant's left hand. The electrodes were connected to a custom-built battery powered bridge which was connected to a Grass 7 DAG pre-amplifier with a recording sensitivity of 0.02 [[micro]seconds]/mm pen deflection. Respiration was recorded using a Phipps and Bird pneumatic bellows connected to a Grass 7PRTE transducer and 7 DAG pre-amplifier.

The stimulus was a 100 Hz tone presented binaurally though Sony DR-7 stereophonic headphones. It had an intensity of 70 dB(SPL) which was calibrated by a Bruel and Kjaer model 2205 sound level meter placed 1 cm from the headphone speaker. Stimulus presentation was controlled by an IBM compatible personal computer. The stimulus duration was 0.1 seconds with a 0 ms risetime for all presentations.

Procedure

On arrival at the laboratory participants were informed that electrodermal activity and respiration measurements would be taken. Alternate participants were assigned to either contextually cued or noncontextually cued conditions.

Participants in the contextually cued condition were instructed:

When you are in the participant room you will hear some tones made by the ticking of a clock. You do not have to make any conscious response to the ticking because we are interested in the automatic responses made by your skin during the experiment rather than your conscious responses. You can simply sit and relax and listen to the ticking. You may close your eyes if you wish.

Participants in the non-contextually cued condition were instructed:

When you are in the participant room you will hear some tones. You do not have to make any conscious response to the tones because we are interested in the automatic responses made by your skin during the experiment rather than your conscious responses. You can simply sit and relax and listen to the tones. You may close your eyes if you wish.

Participants were seated in a semi-reclined padded chair in a darkened room with an ambient temperature of 23 [degrees] C and an illumination level of 0.2 cd/[m.sup.2]. The stimulus presentation and response recording equipment was situated in an adjoining room.

Prior to the experiment participants were informed that the first part of the experiment would be a rest period during which they were to relax. The 4.5 minute pre-stimulation period consisted of a 1.5 minute period to allow the experimenter to stabilize the recording, and a 3 minute period in which nonspecific responses (NSR) would be counted to give an index of participant lability.

The experiment began with 80 stimulus presentations with an onset to onset ISI of 1 second, before the stimulus was omitted for the first time. There were then three repetitions of the experimental block described below.

Each of the three repetitions of the experimental block consisted of the following components. (1) A constant ISI series consisting of 40 stimulus presentations at the 1 second onset to onset ISI. (2) An omission period consisting of an 8.9 second non-stimulation period corresponding to the omission of eight stimulus presentations and ensuring the re-presentation of the next stimulus is in phase with the previous constant ISI series. (3) A second constant ISI series identical to the first. (4) A variable ISI series consisting of 40 stimuli presented with varying ISis of either 0.5, 1 or 1.5 seconds. Over the 40 trials each participant received 12 ISis of 0.5 seconds, 15 ISIs of 1 second and 12 ISIs of 1.5 seconds, giving an average ISI of 1 second. The order of ISis was devised by random draw and was the same for all participants: 0.5, 1, 1.5, 1.5, 0.5, 1.5, 1, 1, 0.5, 1, 0.5, 1, 1.5, 1.5, 0.5, 1.5, 1, 1, 0.5, 1, 0.5, 1, 1.5, 1.5, 0.5, 1.5, 1, 1, 0.5, 1, 0.5, 1, 1.5, 1.5, 0.5, 1.5, 1, 1, 0.5. (5) An 8.9 second omission period.

The third block was followed by a further 40 presentations of the stimulus at a constant onset to onset ISI of 1 second. This series provided the post-omission presentations for the third variable ISI omission block.

Scoring

The short ISis used in this experiment precluded the scoring of SCRs for each individual stimulus presentation. Rather, the scoring and analysis consisted of scoring of the maximum SCR response, the number of SCR responses greater than 0.02 [[micro]seconds] and the total amount of SCR response (sum of all responses) within theoretically relevant time windows. The windows for the omission response measurement were the 9 seconds preceding the omission period (either constant or variable ISI), the 9 second omission period and the first 9 seconds of the constant ISI representation series. If the neuronal model was encoding the temporal parameters of the stimulus series than it would be expected that there would be greater SCR activity in both the omission window and the post-omission window, compared to the pre-omission window. It may be further expected that this effect would be more marked when the omission period was preceded by the predictable constant ISI series, rather than when it was preceded by the variable ISI series.

For the constant to variable ISI manipulation the windows were the last 9 seconds of the constant ISI series and the first 9 seconds of the variable ISI series. Each of these scoring intervals contained nine tone presentations. If the neuronal model was encoding the temporal properties of the stimulus series it would be expected that there would be an increase in all three SCR measures when the constant ISI series was immediately followed by the variable ISI series.

Electrodermal lability was measured by counting the number of responses greater than 0.02 [[micro]seconds] emitted during the 3 minute pre-stimulation period. The participants were split at the median into electrodermally stabile (low activity) and labile (high activity) groups for analysis.

To reduce skewness square root transformations were performed for both maximum SCR and total SCR indices before analysis. Greenhouse-Geisser epsilon corrections were used for effects containing repeated measures and an alpha level of .05 was used throughout the study.

Results

Stimulus omission

A 2 x 2 x 3 x 2 x 3 instruction (clock, no clock) x electrodermal lability (stabile, labile) x block (first, second, third) x ISI variability (preceded by constant or variable ISI series) x window (pre, omission, re-presentation) mixed model analysis of variance (ANOVA) was performed for each dependent variable (maximum SCR, number of SCRs, total SCR). Clock/no clock and electrodermal lability were between-subjects factors, while the other factors were repeated measures.

The clock/no clock factor had no significant main effect, nor was it implicated in any significant interactions and is not discussed further. Table 1 lists the main effects and interactions that reached or approached statistical significance in the analysis of each dependent variable.

[TABULAR DATA FOR TABLE 1 OMITTED]

It is evident that the pattern of significant effects involving the omission trial manipulation is similar for each dependent variable. Post hoc comparisons were calculated within the ISI variability x window interaction testing the simple main effect of window at each level of variability for each dependent variable. When the preceding stimuli had been presented at a constant ISI there was, for each dependent variable, a significant increase in the SCR measures, compared to the preceding control interval, at both the time of stimulus omission and the time at which the stimulus was re-presented (omission window compared to pre-omission window: SQRT total SCR F(1,44) = 12.37, p = .001, MSE = 0.07; SQRT maximum SCR F(1,44) = 14.74, p = .0005, MSE = 0.05; number of SCR F(1,44) = 14.47, p = .0001, MSE = 0.30; pre-omission window compared to post-omission window: SQRT total SCR F(1,44) = 21.13, p = .0001, MSE = 0.07; SQRT maximum SCR F(1,44) = 24.17, p = .0001, MSE = 0.05; number of SCR F(1,44) = 20.04, p = .0001, MSE = 0.32). If the preceding stimuli were presented at a variable ISI there was no significant increase in response at time of stimulus omission or upon representation of the omitted stimulus. Figure 1 illustrates the activity before, during and after the omission period for both variable and constant ISI conditions for each dependent variable. These results are consistent with the notion that during the presentation of the constant ISI stimulus series the neuronal model encoded the ISI of the stimulus and therefore when the stimulus was omitted there was a disparity between the activity of the neuronal model and the afferent stimulation and orienting responses were elicited. If the preceding stimuli were presented at a variable ISI temporal encoding in the neuronal model did not occur to the same extent, and thus the disparity between the activity of the neuronal model and the afferent stimulation was not as great at the time of stimulus omission as in the constant ISI condition. it can also be seen in Fig. 1 that the activity in the pre-block prior to the stimulus omission was higher for the variable ISI condition than the constant ISI condition for each index. These differences were significant for the number of SCR (F(1,44) = 5.19, p = .03, MSE = .32) and maximum SCR (F(1,44) = 4.49, p = .04, MSE = 0.05) indices and closely approached significance for the total SCR measure (F(1,44) = 3.35, p = .07, MSE = 0.07). The differences in pre-omission activity between the variable and constant ISI conditions are consistent with the idea that the variable ISI series results in less complete habituation than the constant ISI series. While it may have been desirable for responses preceding both the constant and variable ISI omission windows to be equal, it is unlikely that this could be achieved with an equal number of stimulus presentations. If it could be achieved it would require a greater number of stimulus presentations in the variable ISI series than in the constant ISI series, a manipulation which would bring its own theoretical and analytical problems.

The presence of a significant block x ISI variability interaction in the case of total SCR activity is due to increased SCR activity on the three omission trials following the constant ISI series compared to those following variable ISI series in the first two experimental blocks but a reversal of this effect on the third experimental block. Given the failure of the block x ISI variability interaction to reach statistical significance in the cases of maximum SCR activity or SCR number measures, this interaction may be no more than chance variation. It is noted that the variable ISI omission series occurred later than the constant ISI omission series within the same block. A counterbalanced design would have alleviated this confound but it seems unlikely that the current design could be the sole reason for the observed results.

The significant main effects for electrodermal lability for each dependent variable were due to the labile participants showing more average electrodermal activity for each measure. There was no evidence that electrodermal lability significantly interacted with any other factors.

In summary, the stimulus omission results indicated that following the constant ISI stimulus series the size and number of SCRs increased both during periods of complete stimulus omission and on re-presentation of the omitted stimulus. There was no evidence of a significant increase in activity if the preceding stimuli had been presented at a variable ISI.

Constant ISI vs. variable ISI stimuli series

To assess the effect of changing (without an intervening omission period) from stimuli presented at a constant ISI to the same stimulus presented at a variable ISI 2 x 2 x 2 x 3 instruction (clock, no clock) x electrodermal lability (stabile, labile) x ISI (constant/variable) x experimental block (1, 2, 3) mixed modal ANOVAs were performed for each dependent variable. Clock/no clock and electrodermal lability were between-subjects factors while the other factors were repeated measures. The scoring windows were defined as the last 9 seconds of a constant ISI section of the stimulus series and the immediately following 9 seconds the first part of the variable ISI portion of the series.

Results were again very similar for the three dependent variables with the only effects reaching or approaching statistical significance for each dependent variable being the main effects for ISI variability and electrodermal lability. The F and p values for the electrodermal lability main effect were: SQRT maximum SCR F(1,22) = 5.43, p = .03, MSE = 0.24; SQRT total SCR F(1,22) = 5.09, p = .03, MSE = 0.27; SCR count F(1,22) = 3.33, p = .08, MSE = .098; indicating generally more electrodermal activity in the labile participants than the stabile ones. Electrodermal lability was not involved in any significant interactions. Table 2 summarizes the magnitude and significance of the ISI variability effect for each dependent variable. These results clearly show that when the ISI of the stimulus series was changed from constant to variable the participants showed an increase in SCR activity reflecting disparity between their previously encoded internal neuronal models and the afferent stimuli.

[TABULAR DATA FOR TABLE 2 OMITTED]

Discussion

The results of this experiment are consistent with a theory of the orienting response in which the neuronal model is capable of encoding the ISI of afferent stimuli, as is the case in comparator theories of habituation. If the orienting response is considered to be a measure of the amount of disparity between the afferent stimulus and the activity of the neuronal model then the results of this experiment can be simply explained. When the stimulus was omitted then there was some disparity between the activity of the neuronal model encoded during the preceding presentations of the stimulus and the afferent stimulus and thus an orienting response was elicited. The omission response is thus a response elicited by the non-presentation of a stimulus and is due entirely to the disparity between the neuronal model and the afferent activity. When the stimulus is represented after the omission period (in phase with previous presentations) the activity of the neuronal model at the time the stimulus is presented is less than it was just before the stimulus was omitted and thus the disparity between the activity of the neuronal model and the afferent re-presented stimulus is greater and a larger orienting response is emitted. The result of this experiment cannot easily be accounted for by dual-process theory (Groves & Thompson, 1970), which does not include a mechanism of encoding the temporal parameters of a stimulus series.

It was noted that the mean number of above-threshold SCRs in each of the scoring is less than 1 in each of the scoring windows in the stimulus omission manipulation, indicating that many participants failed to respond at all in any of these windows. This can be accounted for in a comparator theory of habituation by including a mechanism where a threshold of mismatch is required before a response is emitted, and allowing this threshold to vary between participants.

The results of the manipulation from a fixed to a variable ISI series also suggest that participants encoded the temporal parameters of a stimulus series as it was presented. When the ISI was changed from constant to variable the average size and number of SCRs was increased, consistent with the hypothesis that the afferent stimuli no longer fell at the same time as the peaks in activation encoded by the neuronal model, resulting in an increase in SCR activity. It is possible that the shorter intervals in the current study made it easier for the participants to encode the temporal parameters of a stimulus series and that this is the reason that the current results have been positive where others have not.

The novel scoring technique used in this study may have wider application. With the increasing proliferation of ERP research in psychophysiology it is beneficial that autonomic nervous system research develops in such a way that the measurement of both indices is feasible within a single experiment. Experiments utilizing ERP indices are generally performed at shorter ISis than are experiments using autonomic measures. The measures developed in this investigation provide one way of analysing SCR at shorter ISIs than are commonly used. Further experiments contrasting the validity and parameters of both these techniques as well as alternatives such as that proposed by Barry, Feldmann, Gordon, Cocker & Rennie (1993) are of benefit to the integration of central and autonomic system studies in the future.

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Author:Daniels, Brett A.; Davidson, John A.
Publication:British Journal of Psychology
Date:Aug 1, 1998
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