Effects of stimulus modality and task condition on blink startle modification and on electrodermal responses

Participants in Experiments 1 and 2 performed a discrimination and counting task to assess the effect of lead stimulus modality on attentional modification of the acoustic startle reflex. Modality of the discrimination stimuli was changed across subjects. Electrodermal responses were larger during task-relevant stimuli than during task-irrelevant stimuli in all conditions. Larger blink magnitude facilitation was found during auditory and visual task-relevant stimuli, but not for tactile stimuli. Experiment 3 used acoustic, visual, and tactile conditioned stimuli (CSs) in differential conditioning with an aversive unconditioned stimulus (US). Startle magnitude facilitation and electrodermal responses were larger during a CS that preceded the US than during a CS that was presented alone regardless of lead stimulus modality. Although not unequivocal, the present data pose problems for attentional accounts of blink modification that emphasize the importance of lead stimulus modality.     

The Relationship Between Skin Conductance Orienting the Allocation of Processing Resources

Information processing models of autonomic orienting suggest that the elicitation of an orienting response is associated with either the call for, or the actual allocation of, limited attentional processing resources. However, Dawson, Filion, and Schell (1989) reported a directional dissociation between elicitation of the skin conductance orienting response and resource allocation, as indexed by reaction time slowing on a secondary task. Although larger skin conductance responses were elicited by a task-relevant stimulus than by a task-irrelevant stimulus, reaction time showed the opposite pattern (i.e., greater slowing to secondary task probes presented shortly following the onset of the task-irrelevant stimulus). In the present report, we describe three experiments which examine the generality of this dissociation effect and test specific hypotheses regarding its nature. Results of the first two experiments revealed that the dissociation effect is observed reliably when the task-relevant and task-irrelevant stimuli consist of left ear and right ear tones or high and low pitched binaural tones, across a range of secondary task probe presentation times. However, the third experiment demonstrated that when task-relevant and task-irrelevant stimuli are presented to different sensory modalities (auditory and visual), orienting and resource allocation are both greater during the task-relevant than the task-irrelevant stimuli, thus eliminating the dissociation effect. These results support the hypothesis that the dissociation effect is due to a switch of attention initiated because of the physical similarity of the task-relevant and task-irrelevant stimuli, and suggest that there is a fundamentally positive relationship between skin conductance orienting and resource allocation under selective attention conditions.     

The effect of warning stimulus modality on blink startle modification in reaction time tasks

The present study investigated the effects of lead stimulus modality on modification of the acoustic startle reflex during three reaction time tasks. In Experiment 1, participants (N = 48) were required to press a button at the offset of one stimulus (task relevant) and to ignore presentations of a second (task irrelevant). Two tones that differed in pitch or two lights served as signal stimuli. Blink startle was elicited during some of the stimuli and during interstimulus intervals. Skin conductance responses were larger during task-relevant stimuli in both groups. Larger blink facilitation during task-relevant stimuli was found only in the group presented with auditory stimuli, whereas larger blink latency shortening during task-relevant stimuli was found in both groups. Experiment 2 (N = 32) used only a task-relevant stimulus. Blink magnitude facilitation was significant only in the group presented with tones, whereas blink latency shortening was significant in both groups. Experiment 3 (N = 80) used a go/nogo task that required participants to press a button if one element of a compound stimulus ended before the second, but not if the asynchrony was reversed. The offset asynchrony was varied between groups as a manipulation of task difficulty. Startle magnitude facilitation was larger during acoustic than during visual stimuli and larger in the easy condition. The present data indicate that startle facilitation in a reaction time task is affected by stimulus modality and by task demands. The effects of the task demands seem to be independent of lead stimulus modality.     

The effect of stimulus modality and task difficulty on attentional modulation of blink startle

The effects of the sensory modality of the lead stimulus and of task difficulty on attentional modulation of the electrical and acoustic blink reflex were examined. Participants performed a discrimination and counting task with either two acoustic, two visual, or two tactile lead stimuli. In Experiment 1, facilitation of the electrically elicited blink was greater during task-relevant than during task-irrelevant lead stimuli. Increasing task difficulty enhanced magnitude facilitation for acoustic lead stimuli. In Experiment 2, acoustic blink facilitation was greater during task-relevant lead stimuli, but was unaffected by task difficulty. Experiment 3 showed that a further increase in task difficulty did not affect acoustic blink facilitation during visual lead stimuli. The observation that blink reflexes are facilitated by attention in the present task domain is consistent across a range of stimulus modality and task difficulty conditions.     

The effect of unconditional stimulus modality and intensity on blink startle and electrodermal responses

Attentional accounts of blink facilitation during Pavlovian conditioning predict enhanced reflexes if reflex and unconditional stimuli (US) are from the same modality. Emotional accounts emphasize the importance of US intensity. In Experiment 1, we crossed US modality (tone vs. shock) and intensity in a 2 × 2 between-subjects design. US intensity but not US modality affected blink facilitation. In Experiment 2, we demonstrated that the results from Experiment I were not due to the motor task requirements employed. In Experiment 3, we used a within-subjects design to investigate the effects of US modality and intensity. Contrary to predictions derived from an attentional account, blink facilitation was larger during conditional stimuli that preceded shock than during those that preceded tones. The present results are not consistent with an attentional account of blink facilitation during Pavlovian conditioning in humans.     

Fear potentiated startle at short intervals following conditioned stimulus onset during delay but not trace conditioning

The latency of conditioned fear after delay and trace conditioning was investigated. Some argue that delay conditioning is not dependent on awareness. In contrast, trace conditioning, where there is a gap between the conditioned stimulus (CS) and the unconditioned stimulus (US), is assumed to be dependent on awareness. In the present study, a tone CS signaled a noise US presented 1000 ms after CS onset in the delay conditioning group. In the trace conditioning group, a 200-ms tone CS was followed by an 800-ms gap prior to US presentation. Fear-potentiated startle should be seen at shorter intervals after delay conditioning compared to trace conditioning. Analyses showed increased startle at 30, 50, 100, and 150 ms after CS onset following delay conditioning compared to trace conditioning. This implies that fear-relevant stimuli elicit physiological reactions before extended processing of the stimuli occur, following delay, but not trace conditioning.     

The effect of emotional and attentional load on attentional startle modulation

The interactive effects of emotion and attention on attentional startle modulation were investigated in two experiments. Participants performed a discrimination and counting task with two visual stimuli during which acoustic eyeblink startle-eliciting probes were presented at long lead intervals. In Experiment 1, this task was combined with aversive Pavlovian conditioning. In Group Attend CS+, the attended stimulus was followed by an aversive unconditional stimulus (US) and the ignored stimulus was presented alone whereas the ignored stimulus was paired with the US in Group Attend CS−. In Experiment 2, a non-aversive reaction time task US replaced the aversive US. Regardless of the conditioning manipulation and consistent with a modality non-specific account of attentional startle modulation, startle magnitude was larger during attended than ignored stimuli in both experiments. Blink latency shortening was differentially affected by the conditioning manipulations suggesting additive effects of conditioning and discrimination and counting task on blink startle.     

Effects of conditioned stimulus pre-exposure on human electrodermal conditioning to fear-relevant and fear-irrelevant stimuli

The effects of conditioned stimulus (CS) pre-exposure and fear-relevance of the CS on human Pavlovian electrodermal conditioning were investigated. A differential delayed conditioning paradigm was used with a CS-unconditioned stimulus (US; shock) interval of 8 s. In Experiment 1, 64 subjects were randomized into four groups, two of which received fear-relevant stimuli and the other two fear-irrelevant stimuli. Half of the subjects were pre-exposed to the to-be-CSs and the other half to two not-to-be-CSs, with 15 exposure of each stimulus. During acquisition, subjects received 8 reinforced and 8 nonreinforced CS+ and CS- trials, and during the extinction phase 15 nonreinforced trials of each CS. Pre-exposure to the to-be-CSs retarded conditioning for the first and second interval anticipatory responses (FIRs and SIRs); that is, a latent inhibition effect was demonstrated, although the results for the FIR were inconclusive. The expected effects of fear-relevance were not revealed. Experiment 2 addressed the question whether the long pre-exposure period interfered with the frequently observed "preparedness effect" of higher resistance to extinction to fear-relevant stimuli. The design was similar to that of Experiment 1, but for half of the subjects the acquisition phase was initiated immediately after a short rest period, and for the other half acquisition started after an extended rest period, equal to the duration of the pre-exposure phase in Experiment 1. Twenty extinction trials of each CS were presented. A reliable difference in arousal in terms of spontaneous fluctuations was produced by the rest periods, but although differential conditioning was observed, no effect of fear-relevance was seen during extinction.     

A Comparison of Two Model Systems of Associative Learning: Heart Rate and Eyeblink Conditioning in the Rabbit

In four classical conditioning experiments heart period and eyeblink responses were assessed concomitantly. The conditioned stimuli (CSs) were tones and the unconditioned stimulus (UCS) was a brief paraorbital electric shock. Using a 0.5-s duration CS, bradycardiac conditioned responses that consisted of a 4–5 ms change from pre-CS baseline occurred within 10–20 CS-UCS presentations. However, eyeblink conditioned responses began to occur only after 100–150 CS–UCS presentations. A 1.0-s CS duration resulted in bradycardiac conditioned responses of 15–30 ms change from pre-CS baseline, which again reached asymptote within 10–20 trials. Using a 4-s CS duration, in a differential classical conditioning paradigm, heart period discrimination between a reinforced CS+ and a nonreinforced CS? occurred within 10 trials; asymptotic performance of the heart period conditioned response occurred within 15 CS-UCS presentations and consisted of a bradycardiac response of 40–50 ms for the 12th interbeat interval following tone onset. These data thus indicate that these two model systems of mammalian learning (based on heart period and eyeblink responses) show quite different acquisition functions. It is also significant that heart rate slowing always accompanied the eyeblink conditioned responses, even though increases in general electromyographic activity as well as eyeblink conditioned responses were simultaneously observed during CS presentation.     

Early Pavlovian conditioning impairs later Pavlovian conditioning

Four experiments tested the effects in the rat of very early experience with stimuli to be used later for Pavlovian conditioning. Beginning on postnatal Day 12, prior to the development of substantial detection and effective perception of visual and auditory stimuli, rats were given five daily experiences with either lights or tones and a footshock known to be an effective unconditioned stimulus at these ages. Twenty-four hours after the last of these experiences, pairings of either the light or tone and the unconditioned stimulus were given with parameters established to yield a moderate degree of conditioning in untreated preweanlings (Experiment 1). Experiment 2 determined that early experience with paired or unpaired presentations of either the light or tone and the unconditioned stimulus resulted in a failure to condition to these same lights or tones on postnatal Day 17, although nontreated pups from the same litters conditioned quite effectively. Experiment 3 determined that this early conditioning experience with either paired or unpaired presentations of the lights or tones and the unconditioned stimulus yielded impaired conditioning on postnatal Day 17 in the alternative sensory modality as well, although again nontreated siblings conditioned quite effectively. Experiment 4 replicated the results of each of Experiments 2 and 3 and determined in addition that despite the impairment in conditioning that resulted from early paired or unpaired experience with the stimuli of conditioning, early experience with the individual stimuli of conditioning—with only the CS, the US, or the context—did not result in a similar impairment in conditioning. Although the results were unexpected, they may be understood in part in terms of intersensory competition during development, and there is precedent in the literature for similar interfering effects of early learning on later learning in a variety of species. © 1996 John Wiley & Sons, Inc.     

Probing the orienting response with startle modification and secondary reaction time

Current models of orienting suggest a relationship between the orienting response and attentional processing. This relationship was examined using two independent probe techniques to index attentional processing: secondary reaction time and startle eyeblink modification. Twenty-eight college-age subjects received intermixed presentations of to-be-attended and to-be-ignored tones. Skin conductance orienting responses were obtained during a subset of the tones. Each of the remaining tones contained either a secondary reaction time probe at lead intervals of 150 or 2,000 ms or a startle eyeblink probe presented at lead intervals of 120 or 2,000 ms. In addition, reaction time and startle probes also were presented during selected intertone intervals, and responses to these stimuli served as the baselines from which to compare changes in reaction time and blink amplitude produced by the attended and ignored tones. The results revealed that, compared with the ignored tones, the attended tones were associated with larger skin conductance orienting responses, greater blink inhibition at the 120-ms lead interval, greater blink facilitation at the 2,000-ms lead interval, and greater reaction time slowing at the 2,000-ms lead interval. Consistent with previous findings, the ignored tone was associated with greater reaction time slowing than was the attended tone at the 150-ms lead interval. The results support a relationship between elicitation of the skin conductance orienting response and attentional processes and suggest that the secondary reaction time and blink modification techniques may provide unique information regarding this relationship.     

Neural activity in the medial geniculate nucleus during auditory trace conditioning

 In classical trace conditioning the acquisition of a conditioned response (CR) is possible even though an interval (the trace interval) elapses between the conditioned stimulus (CS) and unconditioned stimulus (US). This implies that some neural representation of the CS (the stimulus trace) is able to support association between the two stimuli. The medial geniculate nucleus (MGN), particularly the medial division (mMGN), has been identified as one site in the auditory pathway where associative related changes in neural activity occur. If neurons in the MGN are involved in such a sensory trace and in acquisition of a CR, then it is expected that activity following an acoustic CS should be related to both stimulus and response. This study examined the extracellular activity of single units in the MGN during differential auditory trace conditioning of the rabbit nictitating membrane response (NMR). Two 150-ms tones (600 Hz and 1200 Hz) served as CS+ and CS–, and the US was periorbital electrostimulation. Changes in activity during the stimulus and trace interval were largest in the medial and dorsal MGN divisions on CS+ trials and on trials in which a CR was made. Examination of probe stimuli of short (50 ms) and long (600 ms) duration suggested that both CR latency and activity changes in the trace interval were related to stimulus duration and time-locked to stimulus offset. Comparisons of neural activity on the basis of fast or slow CR responses revealed different patterns of response – activity on fast CR trials was generally greater and tended to occur earlier. These results suggest that MGN neurons are involved in the maintenance of a sensory memory trace and possibly play a part in CR generation and timing. Received: 2 June 1995 / Accepted: 30 August 1996     

Hemispheric Asymmetry in Conditioning to Facial Emotional Expressions

In the present experiment, we report a right hemisphere advantage for autonomic conditioning to facial emotional expressions. Specifically, angry, but not happy, facial expressions showed significantly more resistance to extinction when presented initially to the right as compared to the left hemisphere. Slides of happy and angry faces were used as conditioned stimuli (CS+ and CS-) with shock as the unconditioned stimulus (UCS). Half of the subjects (n = 15) had the angry face as CS+ (and the happy face as CS-), the other half had the happy face as CS+ (and the angry face as CS-). During acquisition, the CSs were presented foveally. During extinction, using the Visual Half-Field (VHF) technique, half of the CS+ and CS- trials were randomly presented in the right visual half-field (initially to the left hemisphere), and half of the trials were presented in the left half-field (initially to the right hemisphere). Stimuli were presented for 210 ms during acquisition, and for 30 ms during extinction. Bilateral skin conductance responses (SCRs) were recorded. The results showed effects of acquisition only for the angry CS+ group. During extinction, there was a significant Conditioning X Half-field interaction which was due to greater SCRs to the CS+ angry face when it was presented in the left half-field. It is concluded that the present results reveal hemisphere asymmetry effects in facial emotional conditioning.     

Effects of an Attention-Demanding Task on Amplitude and Habituation of the Electrodermal Orienting Response

Two experiments were designed to investigate the effects of performance of a central task on habituation of the skin conductance response to task-irrelevant stimuli. In Experiment 1 (N=48), subjects performed a visual monitoring task in which stimuli were presented at either 800 or 1000 msec. Half the subjects in each group received task-irrelevant tones of 70dB while the other half did not. The results indicated that task-irrelevant tones elicited responses that were larger than those associated with performance of the monitoring task itself, and that responses were larger and habituation slower in the high demand (800 msec) condition than in the low (1000 msec). In order to distinguish between different explanations of these results, Experiment 2 (N=64) employed the same central task and utilized an unexpected change in the pitch of the task-irrelevant stimulus after 20 habituation trials. The results indicated that although habituation was again slower in the high demand condition than in the low, change trial responsiveness was less in the former than in the latter. The results are discussed in terms of arousal and information-processing accounts of habituation.     

Is Elicitation of the Autonomic Orienting Response Associated With Allocation of Processing Resources?

Two experiments investigated whether elicitation of the autonomic orienting response is associated with active allocation of processing resources as indexed by the slowing of reaction time to secondary task probes. In Experiment 1, 75 college student subjects performed a dual task consisting of a primary auditory orienting task and a concurrent secondary visual reaction time task. The primary orienting task included task-relevant tones presented to one car and task-irrelevant tones presented to the other ear. The last trial of the primary task included an unexpected novel tone presented binaurally. The secondary task consisted of a series of brief light flashes presented at critical times throughout the primary task; the reaction time of the subjects' motor responses to these flashes was measured. Consistent with the resource allocation view of orienting, the results demonstrated that resources were allocated during the primary task tones and the novel tone, and this allocation was greater during the early trials than the late trials of the primary task. However, a directional dissociation was observed in that resource allocation was greater during the task-irrelevant tone whereas autonomic orienting responses were larger to the task-relevant tone. Experiment 2 replicated all of these effects and demonstrated that the directional dissociation was sensitive to the predictability and ease of discrimination between the task-relevant and task-irrelevant tones. Taken together, these findings indicate that the relationship between resource allocation and autonomic orienting is a reliable but complex one in need of further research.     

Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response

Rabbits received classical conditioning of the nictitating membrane response (NMR) in a trace conditioning paradigm. In this paradigm, a 250-ms tone conditioned stimulus (CS) occurs, after which there is a 500-ms period of time in which no stimuli occur (the trace interval), followed by a 100-ms air puff unconditioned stimulus (UCS). In Experiment 1, lesions of the hippocampus or cingulate/retrosplenial cortex disrupted acquisition of the long-latency or adaptive conditioned response relative to unoperated controls and animals that received neocortical lesions that spared the cingulate/retrosplenial areas. When animals with hippocampal or cingulate/retrosplenial lesions were switched to a standard delay paradigm in which the CS and UCS were contiguous in time, they acquired in about the same number of trials as naive rabbits. In a second experiment multiple-unit activity in area CA1 of the hippocampus was examined during acquisition of the trace conditioned response (CR). Three groups of animals were tested: animals that had a 500-ms trace interval (Group T-500), animals that received explicitly unpaired presentations of the CS and UCS (Group UP), and animals that underwent conditioning with a 2,000-ms trace interval (Group T-2000). Animals in Group T-500 acquired the CR in about 500 trials. Early in training, and well before any CRs occurred, there was a substantial increase in neuronal activity in the hippocampus that began during the CS and persisted through the trace interval. There was also an increase in the UCS period that modeled the amplitude-time course of the behavioral unconditioned response. Later in conditioning as CRs emerged, there was no longer neuronal bursting throughout the CS + trace period. Rather, the activity shifted to later in the trace interval and formed a model of the amplitude-time course of the behavioral CR. Activity during the UCS period was similar to that seen earlier in conditioning. Animals in Group UP showed no behavioral conditioning and no increase in neuronal activity. Animals in Group T-2000 showed no long-latency behavioral conditioning and no increase in neuronal activity. The data are discussed in terms of the role of the hippocampus in conditioning during situations in which the CS and UCS are not contiguous in time.     

Stimulus Rise Time, Intensity, and Bandwidth Effects on Acoustic Startle Amplitude and Probability

The amplitude and probability of periorbital EMG responses were assessed for a variety of stimuli. In Experiment 1, 50-ms duration broadband noise (20–20K Hz) and tones (1000 Hz), at 95 and 100 dB(A), with rise/fall times of 2.5, 10, and 25 ms, were presented. Noise stimuli were more effective than tones for both response amplitude and probability. Stimulus intensity affected both measures for tones, but only response amplitude for noise. Increasing stimulus rise/fall time had no significant effect for noise, but resulted in lower probability for tones. In Experiment 2, 50-ms duration 1000 Hz tones, at 98 and 102 dB(A), with rise/fall times of 1, 2.5, 5, and 10 ms were presented. Response amplitude was not affected by rise/fall time changes, but increasing rise/fall time from 5 to 10 ms resulted in lower probability. These data show that the startle response can reflect manipulations of stimulus bandwidth, intensity, and rise/fall time, and that startle amplitude and probability reflect these manipulations in different ways. The two response measures may indicate the activity of partially independent underlying mechanisms, with a startle “trigger’ determining response probability and a startle “amplifier’ determining response amplitude for suprathreshold stimuli.     

Effects of Conditioned Stimulus Fear-Relevance and Preexposure on Expectancy and Electrodermal Measures of Human Pavlovian Conditioning

The present research investigated the effects of fear-relevance of the conditioned stimulus (CS) and CS preexposure on human electrodermal conditioning and on a continuous measure of expectancy of the unconditioned stimulus (US). Both experiments employed 20 preexposure, 8 acquisition, and 8 extinction trials in a differential Pavlovian conditioning paradigm with shock as the US. In Experiment 1 (N = 48), electrodermal conditioning was retarded by CS preexposure, but was not influenced by fear-relevance of the CS. Expectancy of the US was retarded by preexposure only in the fear-relevant condition. In Experiment 2 (N = 48), the CS/US contingencies was embedded in a visual masking task. Preexposure retarded both electrodermal conditioning and US expectancy. Neither measure was influenced by fear-relevance of the CS. However, fewer subjects in the preexposure condition learned the CS/US relationship and those who did, did so on later trial than those in the no-preexposure condition. Thus, the results indicated clear retardation of conditioning as a result of preexposure, but no reliable effect of fear-relevance.     

Ontogeny of delay versus trace eyeblink conditioning in the rat

The ontogeny of delay versus trace eyeblink conditioning was examined in 19-, 23-, and 30-day-old rat pups. Pairings of a tone conditioned stimulus (CS) and periocular shock unconditioned stimulus (US; 100-ms) were presented in one of three conditioning paradigms: standard delay [380-ms CS, 280-ms interstimulus interval (ISI)], trace (380-ms CS, 500-ms trace interval), or long-delay (980-ms CS, 880-ms ISI). The results of two experiments indicated that standard delay conditioning emerged between 19 and 23 days of age whereas trace and long-delay eyeblink conditioning emerged more slowly from postnatal Days 19 to 30. Because the acquisition profile for long-delay paralleled that of trace and not standard delay, it appears that the relative deficits in the emergence of trace eyeblink conditioning during development reflect difficulty in forming associations over long ISIs rather than the short-term memory demands of the trace conditioning paradigm.     

Auditory Discrimination and the Eyeblink

This experiment evaluated the association between blinking and cognitive activities. Subjects received 200 and 400 ms tones (1 KHz) at fixed intervals in a duration discrimination paradigm. One group (“Task”) was instructed to respond to the stimuli on the basis of duration and another (“No-Task”) was instructed to ignore the stimuli. Blink activity (latency, rate, duration) and performance (RT, hit and false alarm rates) measures were evaluated. A first analysis (Task subjects only) indicated that stimulus duration had significant effects on RT and blink latency; both were generally longer following the 400-ms than the 200-ms stimuli. In a second analysis, involving Task and No-Task subjects, blink latencies were shorter in the Task group. Blink and eyelid closure durations increased over the task period in both analyses. These effects suggest that blinks occur when attentional processes wane.