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Haloperidol Impairs Learning and Error-Related Negativity in Humans

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Haloperidol Impairs Learning and Error-Related Negativity in Humans Haloperidol Impairs Learning and Error-related Negativity in Humans Patrick J. Zirnheld, Christine A. Carroll, Paul D. Kieffaber, Brian F. O’Donnell, Anantha Shekhar, and William P. Hetrick Abstract & Humans are able to monitor their actions for behavioral Performance Task, the Eriksen Flanker Task, and a learning- conflicts and performance errors. Growing evidence suggests dependent Time Estimation Task. Haloperidol significantly that the error-related negativity (ERN) of the event-related attenuated ERN amplitudes recorded during the flanker task, cortical brain potential (ERP) may index the functioning of impaired learning of time intervals, and tended to cause this response monitoring system and that the ERN may de- more errors of commission, compared to placebo, which pend on dopaminergic mechanisms. We examined the role did not significantly differ from diphenhydramine. Drugs of dopamine in ERN and behavioral indices of learning by had no significant effects on the stimulus-locked P1 and N2 administering either 3 mg of the dopamine antagonist (DA) ERPs or on behavioral response latencies, but tended to af- haloperidol (n = 17); 25 mg of diphenhydramine (n = 16), fect post-error reaction time (RT) latencies in opposite ways which has a similar CNS profile but without DA proper- (haloperidol decreased and diphenhydramine increased ties; or placebo (n = 18) in a randomized, double-blind RTs). These findings support the hypothesis that the DA manner to healthy volunteers. Three hours after drug ad- system is involved in learning and the generation of the ministration, participants performed a go/no-go Continuous ERN. & INTRODUCTION subjects need to have learned a representation of the Humans are able to monitor their actions for behavioral goal behavior for this negativity to be observed conflicts and performance errors, and then modify (Holroyd & Coles, 2002; Dehaene et al., 1994). Increased subsequent behavior accordingly. Growing evidence amplitude of the ERN may index the occurrence of a suggests that the negativity error (Ne; Falkenstein, discrepancy, or mismatch, between the neural represen- Hohnsbein, Hoormann, & Blanke, 1990) or error-related tations of a given response (e.g., an erroneous response) negativity (ERN; Gehring, Coles, Meyer, & Donchin, compared to the neural representations of the required 1990) of the event-related cortical brain potential (ERP) response on a given experimental trial (Falkenstein, may index the functioning of such a monitoring system. Hoorman, et al., 2000; Falkenstein et al., 1990). There is The Ne/ERN is a negative deflection of the ERP that is evidence that the ERN indicates when the consequences more pronounced on incorrect compared to correct of a response are worse than expected (Holroyd & Coles, trials. This negative-going, frontocentral component (De- 2002). Although emotional engagement in a task may haene, Ponser, & Tucker, 1994) peaks about 50 to facilitate ERN amplitude (Dikman & Allen, 2000), con- 80 msec after a response (Falkenstein et al., 1990; scious awareness of a response error is not necessary Gehring et al., 1990) and may be obtained by averaging for the manifestation of an ERN (Nieuwenhuis, Ridder- the response-locked ERPs for incorrect trials alone (Fal- hinkhof, Bloom, Band, & Kok, 2001; Falkenstein, Hoor- kenstein, Hoormann, Christ, & Hohnsbein, 2000; man, et al., 2000) and faked mistakes do not elicit the ERN Scheffers, Coles, Bernstein, Gehring, & Donchin, 1996; (Stemmer, Witzke, & Scho¨nle, 2001). However, whether Gehring, Goss, Coles, Meyer, & Donchin, 1993). Inter- the ERN represents an error detection process (Gehring estingly, the Ne/ERN appears to index the subjective et al., 1993; Falkenstein et al., 1990), a response evalua- sense that a mistake has been made and is not necessarily tion process (Vidal, Hasbroucq, Grapperon, & Bonnet, indicative of an objectively quantified error (Falkenstein, 2000), or a conflict detection process (see Botvinick, Hoorman, et al., 2000; Scheffers & Coles, 2000). However, Braver, Barch, Carter, & Cohen, 2001, for a review) is still unresolved. Nevertheless, several factors appear critical to the elicitation of the ERN, including knowl- Indiana University edge of the goal behavior (Holroyd & Coles, 2002; D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:6, pp. 1098–1112 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929041502779 by guest on 26 September 2021 Dehaene et al., 1994) and a subjective sense of inaccu- the outcome, with greater negative valence yielding rate performance (Scheffers & Coles, 2000). larger ERN amplitudes, and (2) ERN amplitude is larger Investigations of the anatomical origin of the ERN are to infrequent negative outcomes than to frequent neg- informative about candidate neural systems involved ative outcomes, because infrequent negative outcomes in response monitoring, including neural pathways and tend to be less predictable. Thus, ERN appears to reflect neurotransmitters. The anterior cingulate cortex and the a valence-sensitive updating process associated with supplementary motor area have been repeatedly identi- learning. Based on these cumulative findings, as well fied as possible sources of the ERN (Mathalon, Faust- as animal data (see Schultz, Dayan, & Montague, 1997, man, Gray, Askari, & Ford, 2002; Dikman & Allen, 2000; for a review) and results from previous computer mod- Luu, Collins, & Tucker, 2000; Holroyd, Dien, & Coles, els of reinforcement learning using the temporal differ- 1998; Dehaene et al., 1994). Consistent with these ob- ence algorithm (Sutton & Barto, 1998), Holroyd and servations, studies of patients with lesions in either the Coles (2002) compellingly articulated a model in which anterior cingulate cortex (Stemmer, Segalowitz, Witzke, they proposed ‘‘(i) that the ERN reflects the transmis- Lacher, & Scho¨nle, 2000) or the dorsolateral prefrontal sion of a reinforcement signal to the anterior cingulate, cortex (Gehring & Knight, 2000) indicate that both (ii) that this error signal is carried by the mesencephalic cortices are necessary for the generation of a normal dopamine system, and (iii) that it is used to train the ERN. Holroyd, Praamstra, Plat, and Coles (2002) rea- anterior cingulate cortex to optimize performance on soned that because the cingulate sulcus is the only the task at hand’’ (p. 686). Indeed, they reviewed that horizontal part of the medial frontal lobe and ERPs the putative ERN source generators, such as the cingu- are primarily generated by postsynaptic potentials, the late cortex and the medial prefrontal cortex, are densely vertical orientation and large size of apical dendrites innervated by dopamine terminals coming from the in this region make the cingulate sulcus a primary can- ventral tegmental area (VTA) (Carr & Sesack, 2000; didate as the ERN generator. Luu and Tucker (2001) Haber & Fudge, 1997; Heimer et al., 1997). In addition, attributed the genesis of the ERN to an asynchrony the medial prefrontal cortex directly projects to the between a midline theta wave oscillation arising from VTA (Au-Young, Shen, & Yang, 1999; Sesack & Pickel, the centro-medial frontal cortex and a lateral theta 1992; Phillipson, 1979) and the cingulate cortex projects wave oscillation arising from the sensory motor cortices. to the VTA via the nucleus accumbens (Haber & Fudge, They argue in favor of the involvement of the anterior 1997; Heimer et al., 1997). cingulate and supplementary motor cortices in the origin Not only do the putative neuronal source generators of the centro-medial oscillation, which would reflect of the ERN and the neural pathways among related ‘‘response checking’’ (prefrontal) and ‘‘error output’’ structures implicate the dopamine system, but findings (anterior cingulate). from behavioral studies of learning and attention con- In addition to the ‘‘classical’’ ERN, which appears verge on the role of dopamine in attention and learning when subjects experience the subjective sense of having (Margolin, 1978). For example, deficits in procedural made a mistake but have not yet received feedback learning have been observed in both Parkinsonian pa- about their performance, a feedback-related negativity tients (Wallesch et al., 1990) and in normal controls after (FRN) is observed after feedback to incorrect perfor- a small dose of haloperidol (Kumari et al., 1997). Dex- mance (Miltner, Braun, & Coles, 1997). Interestingly, troamphetamine, which increases dopamine synaptic source localization analyses also place the FRN in the release, improves measures of attention and procedural area of the anterior cingulate (Miltner et al., 1997). This learning (Kumari et al., 1997). Furthermore, the dopa- negative-going ERP component, which appears after mine reuptake inhibitors dextroamphetamine and meth- negative feedback, has also been reported by several ylphenidate have both been found to improve attention others (Gehring & Willoughby, 2002; Holroyd & Coles, in patients with attention deficit hyperactivity disorder 2002; Nieuwenhuis et al., 2002; Masaki, Tanaka, Takasa- (Spencer et al., 1995; Arnold, Christopher, Huestis, & wa, & Yamazaki, 2001; Tucker, Hartry-Speicer, McDou- Smeltzer, 1978), and bromocriptine, a direct dopamine gal, Luu, & deGrandpre, 1999; Takasawa, Takino, & agonist, improved verbal learning in a patient who Yamazaki, 1990). Taken together, the evidence indicates sustained a lesion that interrupted dopaminergic path- that the ERN and the FRN index the extent to which a ways
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