Time Course of Error-Potentiated Startle and its Relationship to Error-Related Brain Activity
Abstract
Errors are aversive, motivationally-salient events which prime defensive action. This is reflected in a potentiated startle reflex after the commission of an error. The current study replicates and extends previous work examining the time course of error-potentiated startle as a function of startle lag (i.e., 300 ms or 800 ms following correct and error responses). In addition, the relationship between error-potentiated startle and error-related brain activity in both the temporal (error-related negativity, ERN/Ne) and spectral (error-related theta and delta power) domains was investigated. Event-related potentials (ERPs) were recorded from 32 healthy undergraduates while they performed an arrowhead version of a flanker task. Complex Morlet wavelets were applied to compute oscillatory power in the delta- and theta-band range. Consistent with our previous report, startle was larger following errors. Furthermore, this effect was evident at both early and late startle probe times. Increased delta and theta power after an error was associated with larger error-potentiated startle. An association between ERN amplitude and error-potentiated startle was only observed in a subgroup of individuals with relatively large ERN/Ne amplitude. Among these individuals, ERN/Ne magnitude was also related to multiple indices of task performance. This study further supports the notion that errors are aversive events that prime defensive motivation, and that error-potentiated startle is evident beyond the immediate commission of an error and can be predicted from error-related brain activity.
References
2010). Functional 5-HT1a receptor polymorphism selectively modulates error-specific subprocesses of performance monitoring. Human Brain Mapping, 31, 621–630. doi: 10.1002/hbm.20892
(2010). The role of the BDNF Val66Met polymorphism for the synchronization of error-specific neural networks. Journal of Neuroscience, 30, 10727–10733. doi: 10.1523/JNEUROSCI.2493-10.2010
(2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624–652.
(1993). Emotion, novelty, and the startle reflex: Habituation in humans. Behavioral Neuroscience, 107, 970–980.
(2005). When good things go bad: The reflex physiology of defense. Psychological Science, 16, 468–473.
(2006). A multi-process account of startle modulation during affective perception. Psychophysiology, 43, 486–497.
(2009). Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. Journal of Neuroscience, 29, 98–105.
(2007). Neural evidence for enhanced error detection in major depressive disorder. American Journal of Psychiatry, 164, 608–616.
(2005). Anterior cingulate activity during error and autonomic response. Neuroimage, 27, 885–895.
(2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. Journal of Neuroscience, 25, 11730–11737.
(1994). Localization of a neural system for error detection and compensation. Psychological Science, 5, 303–305.
(2008). Overactive performance monitoring in obsessive-compulsive disorder: ERP evidence from correct and erroneous reactions. Neuropsychologia, 46, 1877–1887.
(2010). Performance monitoring and error significance in patients with obsessive-compulsive disorder. Biological Psychology, 84, 257–263.
(1991). Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. Electroencephalography and Clinical Neurophysiology, 78, 447–455.
(2000). ERP components on reaction errors and their functional significance: A tutorial. Biological Psychology, 51, 87–107.
(1993). A neural system for error detection and compensation. Psychological Science, 4, 385–390.
(2000). Action-monitoring dysfunction in obsessive-compulsive disorder. Psychological Science. 1–6.
(2002). Startle reactivity and anxiety disorders: Aversive conditioning, context, and neurobiology. Biological Psychiatry, 52, 958–975.
(1993). Measuring the time course of anticipatory anxiety using the fear-potentiated startle reflex. Psychophysiology, 30, 340–346.
(1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55, 468–484.
(2008). Errors are aversive: Defensive motivation and the error-related negativity. Psychological Science, 19, 103.
(2008). Increased error-related brain activity in pediatric obsessive-compulsive disorder before and after treatment. American Journal of Psychiatry, 165, 116–123.
(2003a). Anxiety and error-related brain activity. Biological Psychology, 64, 77–90.
(2003b). To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. Psychophysiology, 40, 895–903.
(2004). Error-related psychophysiology and negative affect. Brain and Cognition, 56, 189–197.
(2005). On the ERN and the significance of errors. Psychophysiology, 42, 151–160.
(2002). Error-related brain activity in obsessive-compulsive undergraduates. Psychiatry Research, 110, 63–72.
(2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109, 679–709.
(2001). Discrepant target detection and action monitoring in obsessive–compulsive disorder. Psychiatry Research: Neuroimaging, 108, 101–110.
(2009). Error-Related Oscillations Effects of Aging on Neural Systems for Behavioral Monitoring. Journal of Psychophysiology, 23, 216–223. doi: 10.1027/0269-8803.23.4.216
(2005). Aging and error processing – time-frequency analysis of error-related potentials. Journal of Psychophysiology, 19, 289–297. doi: 10.1027/0269-8803.19.4.289
(2001). Enhanced startle reactions to acoustic stimuli in patients with obsessive-compulsive disorder. American Journal of Psychiatry, 158, 134–136.
(1999). Measuring phase synchrony in brain signals. Human Brain Mapping, 8, 194–208.
(2000). Fear and anxiety: Animal models and human cognitive psychophysiology. Journal of Affective Disorders, 61, 137–159.
(2000). Mood, personality, and self-monitoring: Negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. Journal of Experimental Psychology: General, 129, 43–60.
(2001). Regulating action: Alternating activation of midline frontal and motor cortical networks. Clinical Neurophysiology, 112, 1295–1306.
(2004). Frontal midline theta and the error-related negativity: Neurophysiological mechanisms of action regulation. Clinical Neurophysiology, 115, 1821–1835.
(1995). Fear-potentiated startle in posttraumatic stress disorder. Biological Psychiatry, 38, 378–385.
(2008). The error-related negativity (ERN) and psychopathology: Toward an endophenotype. Clinical Psychology Review, 28, 1343–1354.
(2009). The stability of error-related brain activity with increasing trials. Psychophysiology, 46, 957–961.
(2004). The error-related negativity as a state and trait measure: Motivation, personality, and ERPs in response to errors. Psychophysiology, 41, 84–95.
(2010). Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI. Neuropsychologia, 48, 1144–1159. doi: 10.1016/j.neuropsychologia.2009.12.020
(1966). Error correction time without external error signals. Nature, 212, 438.
(2004). The role of the medial frontal cortex in cognitive control. Science, 306, 443–447.
(2011). Overactive error-related brain activity as an endophenotype for obsessive-compulsive disorder: Evidence from unaffected first-degree relatives. American Journal of Psychiatry, 168, 317–324.
(2005). Error-related brain activity in patients with obsessive-compulsive disorder and in healthy controls. Journal of Psychophysiology, 19, 298.
(1999). Wavelet analysis of neuroelectric waveforms: A conceptual tutorial. Brain and Language, 66, 7–60.
(2007). Theta EEG dynamics of the error-related negativity. Clinical Neurophysiology, 118, 645–668.
(2009). Fast and slow brain rhythms in rule/expectation violation tasks: focusing on evaluation processes by excluding motor action. Behavioral Brain Research, 198, 420–428.
(2002). The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiology & Behavior, 77(4–5), 477–482.
(2010). Increased error-related brain activity in generalized anxiety disorder. Biological Psychology, 85, 472–480.
(2012). Integrating multiple perspectives on error-related brain activity: the ERN as a neurobehavioral trait. Motivation and Emotion, 36, 84–100.
(2009). Modulation of the error-related negativity by induction of short-term negative affect. Neuropsychologia, 47, 83–90.
(2009). Negative affect induced by derogatory verbal feedback modulates the neural signature of error detection. Soc Cognitive and Affective Neuroscience, 4(3), 227–237.
(2004). The neural basis of error detection: Conflict monitoring and the error-related negativity. Psychological Review, 111, 931–959.
(2007). Theta phase resetting and the error-related negativity. Psychophysiology, 44, 39–49.
(2004). Parallel systems of error processing in the brain. Neuroimage, 22, 590–602. doi: 10.1016/j.neuroimage.2004.01.040
(