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The Startle Reflex:A Measure of Emotion and “Attention”
John J. Curtin, Ph.D.University of Wisconsin, Madison
REFERENCES
Anthony, B. J. (1985). In the blink of an eye: Implications of the reflex modification for information processing. In P. K. Ackles, J. R. Jennings, & M. G. M. Coles (Eds.), Advances in Psychophysiology (Vol. 1, pp. 167-218). Greenwich, CT: JAI Press
Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1990). Startle reflex modification: Emotion or attention? Psychophysiology, 27, 513-522.
Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1991). Startle and emotion: Lateral acoustic probes and the bilateral blink. Psychophysiology., 28, 285-295.
Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1993). Pictures as prepulse: Attention and emotion in startle modification. Psychophysiology., 30, 541-545.
Bradley, M. M. & Lang, P. J. (2000). Affective reactions to acoustic stimuli. Psychophysiology., 37, 204-215.
Bradley, M. M., Lang, P. J., & Cuthbert, B. N. (1993). Emotion, novelty, and the startle reflex: Habituation in humans. Behavioral Neuroscience., 107, 970-980.
Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1996). Picture media and emotion: Effects of a sustained affective content. Psychophysiology., 33, 662-670.
Bradley, M. M., Lang, P. J., & Cuthbert, B. N. (1993). Emotion, novelty, and the startle reflex: Habituation in humans. Behavioral Neuroscience., 107, 970-980.
Curtin, J. J., Lang, A. R., Patrick, C. J., & Stritzke, W. G. K. (1998). Alcohol and fear-potentiated startle: The role of competing cognitive demands in the stress-reducing effects of intoxication. Journal of Abnormal Psychology, 107, 547-565.
Curtin, J. J., Patrick, C. J., Lang, A. R., Cacioppo, J. T., & Birbaumer, N. (2001). Alcohol affects emotion through cognition. Psychological Science., 12, 527-531.
Cuthbert, B. N., Bradley, M. M., & Lang, P. J. (1996). Probing picture perception: Activation and emotion. Psychophysiology., 33, 103-111.
Cuthbert, B. N. Schupp, H., Bradley, M., McManis, M., & Lang P. (1998). Probing affective picturesL Attended startle and tone probes. Psychophysiology, 35, 344-347.
Dichter, G. S., Tomarken, A. J., & Baucom, B. R. (2002). Startle modulation before, during and after exposure to emotional stimuli. International Journal of Psychophysiology., 43, 191-196.
Grillon, C., Davis, M., & Phillips, R. G. (1997). Fear-potentiated startle conditioning in humans: Explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology, 34, 451-458.
Miller, M. W., Curtin, J. J., & Patrick, C. J. (1999). A startle probe methodology for investigating the effects of active avoidance on negative emotional reactivity. Biological Psychology., 50, 235-257.
REFERENCES
Miller, M. W., Patrick, C. J., & Levenston, G. K. (2002). Affective imagery and the startle response: Probing mechanisms of modulation during pleasant scenes, personal experiences, and discrete negative emotions. Psychophysiology, 39, 519-529
Patrick, C. J., Berthot, B. D., & Moore, J. D. (1996). Diazepam blocks fear-potentiated startle in humans. Journal of Abnormal Psychology, 105 , 89-96.
Spence, K. W., & Runquist, W. H. (1958). Temporal effects of conditioned fear on the eyelid reflex. Journal of Experimental Psychology., 55, 613-616.
Stritzke, W. G. K., Patrick, C. J., & Lang, A. R. (1995). Alcohol and human emotion: A multidimensional analysis incorporating startle-probe methodology. Journal of Abnormal Psychology, 104, 114-122.
van-Boxtel, A., Boelhouwer, A. J. W., & Bos, A. R. (1998). Optimal EMG signal bandwidth and interelectrode distance for the recording of acoustic, electrocutaneous and photic blink reflexes. Psychophysiology, 35, 690-697.
Vrana, S. R., Spence, E. L., & Lang, P. J. (1988). The startle probe response: A new measure of emotion? Journal of Abnormal Psychology, 97, 487-491.
REFERENCES
The Startle Reflex and Emotion
Response matching hypothesiso Startle reflex is a defensive response
o The magnitude of the reflex is INCREASED when the organism is fearful (fear potentiated startle; FPS)
o The magnitude of the reflex is DECREASED when the organism is “feeling good”***
Measurement of the Startle Reflex
Measurement
o Elicited with brief burst of white noise (“startle probe”) presented over headphones
o Eyeblink response is indexed by recording electrical activity in the orbicularis oculi muscle
Amygdala
CG LH PVH RPC
Freezing Blood Pressure
Stress Hormones
StartleReflex
Neural Circuitry of Fear, Ledoux et al.,
Amygdala
CG LH PVH RPC
Freezing Blood Pressure
Stress Hormones
StartleReflex
SensoryThalamus
Auditory FearStimulus
Neural Circuitry of Fear, Ledoux et al.,
Amygdala
CG LH PVH RPC
Freezing Blood Pressure
Stress Hormones
StartleReflex
SensoryThalamus
AuditoryCortex
Auditory FearStimulus
Neural Circuitry of Fear, Ledoux et al.,
Amygdala
CG LH PVH RPC
Freezing Blood Pressure
Stress Hormones
StartleReflex
SensoryThalamus
AuditoryCortex
Association Cortex
Auditory FearStimulus
Hippocampal Formation
Neural Circuitry of Fear, Ledoux et al.,
Neural Circuitry of Startle Reflex
Amygdala
Nucleus ReticularisPontis Caudalis (RPC)
Cochlear Root Neurons
Spinal & Facial Motonuerons
Abrupt noise (probe) Startle Reflex
Fear conditioning/Shock sensitization
• Lesions of block FPS• Electrical stim enhances
startle reflex
Fear Conditioning and Startle in Animals
o Brown, Kalish, and Farber (1951) is classic animal studyo Michael Davis and colleagues have demonstrated:
Increased FPS with increased shock intensity Increased FPS with anxiogenics Decreased FPS with anxiolytics
Brown, Kalish, and Farber (1951)
0
10
20
30
Block 1 Block 2 Block 3
Extinction
Control
Fear conditioned
Fear Conditioning and Startle in Humans
Spence & Runquist, 1958o Forward and backward pairing of CS (light) with
shock UCSo Airpuff probes presented at 500 and 4500ms post
CS onseto Measured eyeblink closure
8
10.5
13
15.5
18
0 10 20 30 40
4.5s Forward
4.5s Backward
.5s Forward
.5s Backward
Attentional Modulation of Startle
Attentional effects on reflex magnitudeo Reviewed in Anthony (1985)
o Increased if matches modality of foreground stimuluso Decreased as more attention is directed to
foreground Reaction time task (time course, covary with HR) Interest level (Nudes vs. basket; tones vs. music; faces vs.
blank screen)
Anthony & Graham (1985)
175
200
225
250
275
Match MisMatch
Modality
Bli
nk
mag
. (A
-D u
nit
s)
Simons & Zelson (1985)
100
125
150
Interesting Dull
Foreground Inteserest
Bli
nk
mag
. (A
-D u
nit
s)
Slide Viewing Paradigm
Vrana, Spence, & Lang, 1988o 36 slides (12 pleasant, 12 neutral, 12 unpleasant)o 6s presentation with 16-24s ITIo 9 unpredictable probe presentations within valence and
9 ITI startles
300
350
400
450
Pleasant Neutral Unpleasant
Additional Measures in Slide Viewing
Attention or Emotion in Slide Viewing
Bradley, Cuthbert & Lang (1990)o Compared startle response to acoustic vs. visual
probes during slide viewing
o Regardless of probe modality, same direction of linear valence effect was observed
Acoustic Probes
800
850
900
950
1000
Pleasant Neutral Unpleasant
Visual Probes
440
465
490
515
540
Pleasant Neutral Unpleasant
Lateralization of the Reflex
Bradley, Cuthbert, and Lang (1991)o Monoaural probes to left and right ears during slide
viewing and recorded left and right orbicularis startle response [see also, Bradley, Cuthbert and Lang, 1996]
o No valence modulation elicited by right ear probeso Response is larger on ipsilateral measurement siteo No interaction of measurement site with slide valence
Left Ear Probe
150
200
250
300
Left orbicularis Right orbicularis
PleasantNeutralUnpleasant
Right Ear Probe
150
200
250
300
Left orbicularis Right orbicularis
Pleasant
Neutral
Unpleasant
Attention and Valence in Picture Processing
Cuthbert, Schupp, Bradley, McManis, & Lang (1998)o Tones and probes presented during slide and ITIo Task was to press button to indicate detection of
match (e.g., probe-probe) during ITIo Startle response to probe displays typical valence
effecto P3 to probes (and tones) shows attentional effect to
all affective material
Right Ear Probe
12
16
20
24
Attend/Task No-Task
PleasantNeutralUnpleasant
Startle Response
100
107
114
121
Attend/Task No-task
PleasantNeutralUnpleasant
Imagery and Startle
Miller, Patrick, & Levenston (2002)o Participants trained to image standard or personal
pleasant neutral or unpleasant scripts
-0.3
-0.2
-0.1
0
0.1
0.2
0.3
Exp 1 Exp2:Standard
Exp2:Personal
Blin
k m
ag
(z-
sc
ore
)
Pleasant
Neutral
Unpleasant
Time Course of Response in Slide Viewing
Bradley, Cuthbert, and Lang, 1993o Examined startle across the slide viewing time-courseo Early “pre-pulse”/attentional effects o Later valence effects
3
4
5
6
300 800 1300 3800 6300 9800
Positive
Neutral
Negative
3
4
5
6
Early Late
Positive
Neutral
Negative
Arousal Effects
Cuthbert, Bradley, & Lang, 1996o Varied valence (pleasant, neutral, and unpleasant)
and arousal (3 levels) ratings of slideso 3 probe intensities (80, 95, and 105 dB)o Skin and HR effects vs. Startle effects
Habituation of the Startle Reflex
Bradley, M. M., Lang, P. J., & Cuthbert, B. N. (1993). Emotion, novelty, and the startle reflex: Habituation in humans. Behavioral Neuroscience., 107(6), 970-980.
Previous research with both animal and human Ss has shown that startle reflex magnitude is potentiated in an aversive stimulus context, relative to responses elicited in a neutral or appetitive context. In the present experiment, the same pleasant, unpleasant, and neutral picture stimuli were repeatedly presented to human Ss. Startle reflex habituation was assessed in each stimulus context and was compared with the habituation patterns of heart rate, electrodermal, and facial corrugator muscle responses. All systems showed initial differentiation among affective picture contents and general habituation over trials. The startle reflex alone, however, continued to differentiate among pleasant, neutral, and unpleasant pictures throughout the presentation series. These results suggest that (1) the startle probe reflex is relatively uninfluenced by stimulus novelty, (2) the startle modulatory circuit (identified with amygdala-reticular connections in animals) varies systematically with affective valence, and (3) the modulatory influence is less subject to habituation than is the obligatory startle pathway or responses in other somatic and autonomic systems.
Discrete Periods in Slide Viewing
Dichter, Tomarken, & Baucom, 2002o Examined startle before (1.5-2.5s), during (3.5-4.5s) and
after (1.5-2.5s) a slide viewing periodo Valence cued with arrow followed 4s later by slide
40
45
50
55
60
Positive
Neutral
Negative
Startle and Mood effects
Bradley, Cuthbert, & Lang, 1996o Presented slides blocked on valence (24 per valence)o Examined slide viewing and inter-slide interval
effectso Included startle, corrugator, SC and HR. Also,
affective judgment of words
45
50
55
60
65
70
75
First half Second half
Postive
Neutral
Negative
Startle during Sound Perception
Bradley & Lang, 2000o 60 affective sounds (listen to example)o Visual startle probeso Observed typical linear valence effect for startle
Stress Response Dampening Model
o Alcohol intoxication produces a direct, pharmacological suppression of activity in the defensive (fear/anxiety) system.
o Therefore, alcohol consumption is reinforcing -- particularly when consumed in stressful contexts.
Method
o Standard emotional slide viewing paradigmo 36 slides (12 pos, 12 neut, 12 neg)o Slides presented for 6 seconds
Paradigm
Participantso 36 social drinkers in 2 beverage conditions: Alcohol
(0.075%) and No-alcohol
o Startle responseo Corrugator (frown) EMGo Autonomic measures (SC, HR)o Slide ratings (valence, arousal)
Measures
Stritzke, Patrick, & Lang, (1995). Journal of Abnormal Psychology, 104, 114-122.
Valence Modulated Startle
-2
-1
0
1
2
Pleasant Neutral Unpleasant
Valence
Bli
nk
mag
nit
ud
e (z
-sco
re)
Alcohol does not affect the “valence modulated” startle response. (i.e. sig. linear effect in both groups)
Overall Startle Response
0
4
8
12
No alcohol Alcohol
Beverage condition
Bli
nk
mag
nit
ud
e (m
irco
volt
s)
Alcohol produces a significant reduction in overall blink magnitude (and latency, not displayed).
0
0.1
0.2
0.3
0.4
0.5
0.6
Pleasant Neutral Unpleasant
Valence
SC
R (
mic
rosi
emen
s)
Skin Conductance Response
Alcohol does reduce arousal response, but to all emotional slides, regardless of slide valence.
Diazepam and Startle
-1
-0.5
0
0.5
1
1.5
2
Placebo 10 mg 15mg
Drug condition
Fe
ar
po
ten
tia
tio
n
Patrick, Berthot, & Moore (1996)o Placebo or diazepam (Valium)o Negative and neutral slide viewing paradigmo Dose dependent effect of diazepam on fear
potentiated startle to negative slides
o Alcohol intoxication reduces “attentional capacity” (Alcohol myopia)
o Alcohol focuses attention on the most salient stimuli in the environment
o If the most salient stimulus in the environment is pleasant, stress response will be reduced
o Note: If most salient stimulus is stressor, stress response will be increased
Attention Allocation Model
Participants
Measures
o 48 social drinkers in 2 beverage conditions: Alcohol (0.075%) and No-alcohol
• Startle response• Corrugator (frown) EMG• Autonomic measures (SC, HR)
Curtin, Lang, Patrick, & Stritzke, W. G. K. (1998). Journal of Abnormal Psychology, 107, 547-565.
Method
o 8 blocks alternating between Shock threat and Safe
o 6 positive slides in each block
o 6 startle probes in each block - half during slide presentation (distraction) - half during inter-slide interval (no-distraction)
o Fear poteniated startle (FPS) is the difference between startle response in Shock threat vs. Safe blocks
!- Slide - Startle probe
Key
! ! !! ! ! ! !!
Method
Skin Conductance
-0.15
-0.1
-0.05
0
0.05
0.1
0.15
0.2
No-alcohol Alcohol
mic
rosi
emen
s
Safe
Threat
Corrugator Level
-0.5
-0.25
0
0.25
0.5
No-alcohol Alcohol
mic
rovo
lts
Safe
Threat
Tonic Levels of SC and Corrugator
o Threat manipulation increased SCL and Corrugator level.
o Beverage does not moderate this threat effect.
Skin Conductance
0
2
4
6
8
No-alcohol Alcohol
mic
rosi
emen
s
Safe
Threat
Heart Rate
-8
-6
-4
-2
0
No-alcohol Alcohol
BP
M c
han
ge
Safe
Threat
Corrugator Response
0
0.4
0.8
1.2
No-alcohol Alcohol
mic
rovo
lts
Safe
Threat
Phasic Response to Threat Cue
o Sig. threat effect in phasic response to block onset light cue
o Beverage did not moderate this effect
0
2
4
6
8
10
No-distraction Distraction
FP
S
(mir
covo
lts)
No-alcohol
Alcohol
o In no-distraction condition, sig. FPS observed in both beverage groups.
o In distraction condition, sig. FPS observed only in no-alcohol group.
Threshold for significant FPS
Fear Potentiated Startle
Method
Participants
o 48 social drinkers in 2 beverage conditions Alcohol (0.08%) and No-alcohol
Measures
o Startle responseo Event related potentials (focused on P3)o Task performance
Curtin et al., (2001). Psychological Science
Trial Structure
Startle Shock Button press
S1 ! S2 ^
300ms 1400ms 300ms 200ms 300ms
S1 Threat-focus: Animal/Body-part Divided attention: Animal/Body-part or Animal/Body-part
Method
• 24 blocks of trials (20 trials per block)– 8 Threat-focus blocks– 16 Divided attention blocks
Block Structure
Next Block: SHOCK Only
Read each word as it is presentedShocks to animal words
HEAD
NECK
BEAR
!!!SHOCK!!!
Next Block: TASK & SHOCK
Press button quickly to square after GREEN wordDo not press button after RED word
Shocks to ANIMAL words
HAND
MOUTH
TIGER
!!!SHOCK!!!
10 of 10 responses credited in this block
Fear Potentiated Startle
0
3
6
9
12
No-alcohol Alcohol
FP
S (
mic
rovo
lts)
Threat-focus
Divided attention
o In threat focus, no sig. difference in FPS between beverage groups
o In divided attention, FPS sig. reduced
The Next Logical Step
40
65
90
115
140
No Safety Safety
CSM
CSP
Deliberate Emotion Regulation
50556065707580859095
100
Pre
-re
gu
lati
on
Su
pp
ress
Mai
nta
in
En
han
ce
Neutral
Negative
Deliberate Regulation when Intoxicated
4546474849505152535455
SUPPRESS MAINTAIN ENHANCE4546474849505152535455
SUPPRESS MAINTAIN ENHANCE
Sober Intoxicated (n=3)
Fear vs. Anxiety
Grillon, C., Davis, M., & Phillips, R. G. (1997). Fear-potentiated startle conditioning in humans: Explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology, 34, 451-458.
Conditioned fear in response to explicit and contextual cues was examined using the startle reflex in 3 groups of college students ( N = 58) over 2 sessions separated by 4-5 days. The CS was paired with an aversive unconditioned stimulus (UCS; shock) during conditioning in the paired but not in the unpaired group. In the reaction time (RT) group, the UCS was a nonaversive visual signal for an RT task. In the paired group, the CS potentiated startle in the postconditioning phase. This conditioned response was fully retained over the retention interval. There was no substantial change in baseline startle (startle delivered in the absence of CS). By contrast, startle was not potentiated by the CS in the unpaired group, but baseline startle was increased from Session 1 to Session 2. In the RT group, startle was not affected by the CS, and baseline startle was reduced from Session 1 to Session 2. These results suggest that paired presentations of a CS and an aversive UCS result in conditioned fear in response to the CS but little contextual fear, whereas unpaired presentations of a CS and UCS lead to poor explicit cue conditioning but substantial contextual fear.
Affective Consequences of Active Coping
Miller, Curtin, & Patrick, 1999o Examined active vs. passive coping in a threat paradigm
o 4 groups Active tapping (contingent blasts) Passive tapping (yoked/non-contingent) Passive no-tapping (yoked) Control tapping (no blasts)
o Task included string of 30 asterisks during CS+ and CS- trials: Tapping during CS+ for tapping groups Blasts (.5s, 115dB) during CS+ for threat groups
o Used airpuff as startle probe
Active Avoidance and Behavioral Activation
1514131211109876543210-1.5
-1.0
-0.5
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
Active Tapping CS+
Active Tapping CS-
Passive Tapping CS+
Passive Tapping CS-
Time After CS Onset (s)
HR
Ch
an
ge
(B
PM
)
Active Tapping Passive Tapping Passive No Tapping Control Tapping46
48
50
52
54
CS+CS-
Blin
k M
ag
nit
ud
e (
T-s
co
res
)
Active Avoidance and Behavioral Activation
Emotion and Psychopathy
47
49
51
53
Non-psychopaths Pure antisocial Psychopaths
Bli
nk
mag
. (T
-sco
re)
Pleasant
Neutral
Unpleasant
Patrick, Bradley, & Lang (1993)o Groups did not differ in self-report of emotional
response to the slides
o Psychopaths did not display the typical potentiation of startle to the negatively valent slides
Measurement and Processing Issues
Data acquisitiono Elicited with white noise probe (95 – 105 dB)o Sampled at 1000Hzo Broadband online filter (.015 - 500Hz)o Include habituation probes
Data Processingo Epoch around triggers (-50 to 250ms window)o Bandpass filter (30 - 500Hz; van-Boxtel et al., 1998)o Rectify and lowpass filter (30 Hz)o Baseline correct
Scoring Responseso Max response in 20 – 120 windowo No response trialso Latency of response