Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm

Day, Jeremy J.; Wheeler, Robert A.; Roitman, Mitchell F.; Carelli, Regina M.

doi:10.1111/j.1460-9568.2006.04654.x

Cited by 140Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsNeural and Behavioral Psychology Studies

Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm

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Day, Jeremy J., Wheeler, Robert A., Roitman, Mitchell F., Carelli, Regina M.·2006·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2006.04654.x

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Abstract

Environmental stimuli predictive of appetitive events can elicit Pavlovian approach responses that enhance an organism's ability to track and secure natural rewards, but may also contribute to the compulsive nature of drug addiction. Here, we examined the activity of individual nucleus accumbens (NAc) neurons during an autoshaping paradigm. One conditioned stimulus (CS+, a retractable lever presented for 10 s) was immediately followed by the delivery of a 45-mg sucrose pellet to a food receptacle, while another stimulus (CS-, a separate retractable lever presented for 10 s) was never followed by sucrose. Approach responses directed at the CS+ and CS- were recorded as lever presses and had no experimental consequence. Rats (n = 9) selectively approached the CS+ on more than 80% of trials and were surgically prepared for electrophysiological recording. Of 76 NAc neurons, 57 cells (75%) exhibited increases and/or decreases in firing rate (i.e. termed 'phasically active') during the CS+ presentation and corresponding approach response. Forty-seven percent of phasically active cells (27 out of 57) were characterized by time-locked but transient increases in cell firing, while 53% (30 out of 57) showed a significant reduction in firing for the duration of the CS+. In contrast, the same excitatory subpopulation exhibited smaller increases in activity relative to CS- onset, while the inhibitory subpopulation showed no change in firing during the CS- period. The magnitude and prevalence of cue-related neural responses reported here indicates that the NAc encodes biologically significant, repetitive approach responses that may model the compulsive nature of drug addiction in humans.

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The ventral striatum is implicated in Pavlovian learning.
“Considerable evidence has amassed to implicate the ventral striatum (VS) in Pavlovian learning”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [17]

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The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · see citing works
Dopamine, learning and motivation.
Wise, R. A. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1406 · Cited by 3,379 · cited 2× · see citing works
“Signal-to-baseline (S : B) ratios for CS+ excitatory and CS+ inhibitory populations were computed by dividing the ‘signal’ (firing rate for an individual cell during a single second of the cue period) by the baseline (averaged activity for that cell during the 10 s prior to cue presentation).”
BackgroundMethod
Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex.
Pavlov, P. I. (1930) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1930.02220110256018 · Cited by 2,681 · see citing works
From motivation to action: Functional interface between the limbic system and the motor system
MOGENSON, G., JONES, D., & YIM, C. (1980) · Progress in Neurobiology · doi:10.1016/0301-0082(80)90018-0 · Cited by 2,331 · see citing works
Discrete coding of reward probability and uncertainty by dopamine neurons
Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003) · Science · doi:10.1126/science.1077349 · Cited by 2,085 · see citing works
AUTO‐SHAPING OF THE PIGEON'S KEY‐PECK1
Brown, P. L., & Jenkins, H. M. (1968) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1968.11-1 · Cited by 1,544 · see citing works
Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task
Schultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291 · see citing works
Specificity in the projection patterns of accumbal core and shell in the rat
Heimer, L., Zahm, D. S., Churchill, L., Kalivas, P. W., & Wohltmann, C. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90202-y · Cited by 1,219 · see citing works
Subsecond dopamine release promotes cocaine seeking
Phillips, P. E. M., Stuber, G. D., Heien, M. L. A. V., Wightman, R. M., & Carelli, R. M. (2003) · Nature · doi:10.1038/nature01476 · Cited by 1,113 · see citing works
Self-citation
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning
Kelley, A. E. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.11.015 · Cited by 942 · see citing works
Dopamine and drug addiction: the nucleus accumbens shell connection
Di Chiara, G., Bassareo, V., Fenu, S., De Luca, M. A., Spina, L., Cadoni, C., Acquas, E., Carboni, E., Valentini, V., & Lecca, D. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.032 · Cited by 935 · see citing works
Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens
Nicola, S. M., Surmeier, D. J., & Malenka, R. C. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.185 · Cited by 931 · see citing works
Impulsive choice induced in rats by lesions of the nucleus accumbens core
Cardinal, R. N., Pennicott, D. R., Lakmali, C., Sugathapala, Robbins, T. W., & Everitt, B. J. (2001) · Science · doi:10.1126/science.1060818 · Cited by 923 · see citing works
Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Mirenowicz, J., & Schultz, W. (1996) · Nature · doi:10.1038/379449a0 · Cited by 829 · see citing works
The neuropsychological basis of addictive behaviour
Everitt, B. J., Dickinson, A., & Robbins, T. W. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00088-1 · Cited by 808 · see citing works
The nucleus accumbens as a complex of functionally distinct neuronal ensembles: An integration of behavioural, electrophysiological and anatomical data
Pennartz, C. M. A., Groenewegen, H. J., & LOPESDASILVA, F. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90025-6 · Cited by 802 · see citing works
Neuronal activity in monkey ventral striatum related to the expectation of reward
Schultz, W., Apicella, P., Scarnati, E., & Ljungberg, T. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04595.1992 · Cited by 744 · see citing works
Dopamine operates as a subsecond modulator of food seeking
Roitman, M. F., Stuber, G. D., Phillips, P. E. M., Wightman, R. M., & Carelli, R. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3823-03.2004 · Cited by 718 · see citing works
Self-citation
AUTO‐MAINTENANCE IN THE PIGEON: SUSTAINED PECKING DESPITE CONTINGENT NON‐REINFORCEMENT2
Williams, D. R., & Williams, H. G. (1969) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1969.12-511 · Cited by 717 · see citing works
Psychomotor stimulant addiction: a neural systems perspective
Everitt, B. J., & Wolf, M. E. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03312.2002 · Cited by 700 · see citing works
Drug-activation of brain reward pathways
Wise, R. A. (1998) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(98)00063-5 · Cited by 684 · see citing works
Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior
Goto, Y., & Grace, A. A. (2005) · Nature Neuroscience · doi:10.1038/nn1471 · Cited by 576 · see citing works
THE FORM OF THE AUTO‐SHAPED RESPONSE WITH FOOD OR WATER REINFORCERS1
Jenkins, H. M., & Moore, B. R. (1973) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1973.20-163 · Cited by 492 · see citing works
Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output
Roitman, M. F., Wheeler, R. A., & Carelli, R. M. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.055 · Cited by 453 · see citing works
Self-citation
Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network
Pan, W.-X., Schmidt, R., Wickens, J. R., & Hyland, B. I. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1478-05.2005 · Cited by 429 · see citing works
Limbic-Striatal Memory Systems and Drug Addiction
Robbins, T. W. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4103 · Cited by 379 · see citing works
Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings
Nicolelis, M. A. L., Ghazanfar, A. A., Faggin, B. M., Votaw, S. V., & Oliveira, L. M. O. (1997) · Neuron · doi:10.1016/s0896-6273(00)80295-0 · Cited by 376 · see citing works
Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum
Cromwell, H. C., & Schultz, W. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01014.2002 · Cited by 357 · see citing works
Differential involvement of NMDA, AMPA/kainate and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior
Di Ciano, P., Cardinal, R. N., Cowell, R. A., Little, S. J., & Everitt, B. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09471.2001 · Cited by 354 · see citing works
Dopamine and N-Methyl-D- Aspartate Receptor Interactions in the Neostriatum
Cepeda, C., & Levine, M. S. (1998) · Developmental Neuroscience · doi:10.1159/000017294 · Cited by 350 · see citing works
Evidence of a Functional Relationship between the Nucleus Accumbens Shell and Lateral Hypothalamus Subserving the Control of Feeding Behavior
Stratford, T. R., & Kelley, A. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-11040.1999 · Cited by 316 · see citing works
Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical–ventral striatopallidal systems
Parkinson, J. A., Willoughby, P. J., Robbins, T. W., & Everitt, B. J. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.42 · Cited by 314 · see citing works
Evidence That Separate Neural Circuits in the Nucleus Accumbens Encode Cocaine Versus “Natural” (Water and Food) Reward
Carelli, R. M., Ijames, S. G., & Crumling, A. J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04255.2000 · Cited by 310 · see citing works
Self-citation
Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: Further evidence for limbic cortical-ventral striatopallidal systems.
Parkinson, J. A., Willoughby, P. J., Robbins, T. W., & Everitt, B. J. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.1.42 · Cited by 309 · see citing works
Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function
Parkinson, J. A., Dalley, J. W., Cardinal, R. N., Bamford, A., Fehnert, B., Lachenal, G., Rudarakanchana, N., Halkerston, K. M., Robbins, T. W., & Everitt, B. J. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00291-7 · Cited by 288 · see citing works
Influence of Expectation of Different Rewards on Behavior-Related Neuronal Activity in the Striatum
Hassani, O. K., Cromwell, H. C., & Schultz, W. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.6.2477 · Cited by 257 · see citing works
Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study
Usuda, I., Tanaka, K., & Chiba, T. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00359-x · Cited by 248 · see citing works
When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function
Plenz, D. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00196-6 · Cited by 242 · see citing works
The Ventral Tegmental Area Is Required for the Behavioral and Nucleus Accumbens Neuronal Firing Responses to Incentive Cues
Yun, I. A., Wakabayashi, K. T., Fields, H. L., & Nicola, S. M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5282-03.2004 · Cited by 238 · see citing works
Neural Encoding in Ventral Striatum during Olfactory Discrimination Learning
Setlow, B., Schoenbaum, G. M., & Gallagher, M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00264-2 · Cited by 220 · see citing works
Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: Implications for the neurobiology of emotion.
Bussey, T. J., Everitt, B. J., & Robbins, T. W. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.5.908 · Cited by 201 · see citing works
Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats.
Cardinal, R. N., Parkinson, J. A., Lachenal, G., Halkerston, K. M., Rudarakanchana, N., Hall, J., Morrison, C. H., Howes, S. R., Robbins, T. W., & Everitt, B. J. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.4.553 · Cited by 201 · see citing works
Effects of selective excitotoxic lesions of the nucleus accumbens core, anterior cingulate cortex, and central nucleus of the amygdala on autoshaping performance in rats.
Cardinal, R. N., Parkinson, J. A., Lachenal, G., Halkerston, K. M., Rudarakanchana, N., Hall, J., Morrison, C. H., Howes, S. R., Robbins, T. W., & Everitt, B. J. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.4.553 · Cited by 201 · see citing works
Functional Specificity of Ventral Striatal Compartments in Appetitive Behaviors
KELLEY, A. E. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09262.x · Cited by 198 · see citing works
Cue-Evoked Firing of Nucleus Accumbens Neurons Encodes Motivational Significance During a Discriminative Stimulus Task
Nicola, S. M., Yun, I. A., Wakabayashi, K. T., & Fields, H. L. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00657.2003 · Cited by 196 · see citing works
Conditioned Approach and Contact Behavior toward Signals for Food or Brain-Stimulation Reinforcement
Peterson, G. B., Ackilt, J. E., Frommer, G. P., & Hearst, E. S. (1972) · Science · doi:10.1126/science.177.4053.1009 · Cited by 186 · see citing works
Nucleus accumbens cell firing during goal-directed behaviors for cocaine vs. ‘natural’ reinforcement
Carelli, R. M. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00760-6 · Cited by 183 · see citing works
Self-citation
A comparison of nucleus accumbens neuronal firing patterns during cocaine self-administration and water reinforcement in rats
Carelli, R. M., & Deadwyler, S. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07735.1994 · Cited by 180 · see citing works
Self-citation
Electrophysiological and pharmacological evidence for the role of the nucleus accumbens in cocaine self-administration in freely moving rats
Chang, J., Sawyer, S. F., Lee, R., & Woodward, D. J. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01224.1994 · Cited by 177 · see citing works
The attribution of incentive salience to a stimulus that signals an intravenous injection of cocaine
Uslaner, J. M., Acerbo, M. J., Jones, S., & Robinson, T. E. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.02.001 · Cited by 167 · see citing works
Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: Implications for the neurobiology of emotion.
Bussey, T. J., Everitt, B. J., & Robbins, T. W. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.5.908 · Cited by 163 · see citing works
The nucleus accumbens and reward: neurophysiological investigations in behaving animals
Carelli, R. M. (2002) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582302238338 · Cited by 131 · see citing works
Self-citation
Firing of Nucleus Accumbens Neurons During the Consummatory Phase of a Discriminative Stimulus Task Depends on Previous Reward Predictive Cues
Nicola, S. M., Yun, I. A., Wakabayashi, K. T., & Fields, H. L. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00658.2003 · Cited by 131 · see citing works
Firing patterns of nucleus accumbens neurons during cocaine self-administration in rats
Carelli, R. M., King, V. C., Hampson, R. E., & Deadwyler, S. A. (1993) · Brain Research · doi:10.1016/0006-8993(93)90557-4 · Cited by 129 · see citing works
Self-citation
Pavlovian Conditioning with Heat Reinforcement Produces Stimulus-Directed Pecking in Chicks
Wasserman, E. A. (1973) · Science · doi:10.1126/science.181.4102.875 · Cited by 127 · see citing works
Lesions to the subthalamic nucleus decrease impulsive choice but impair autoshaping in rats: the importance of the basal ganglia in Pavlovian conditioning and impulse control
Winstanley, C. A., Baunez, C., Theobald, D. E. H., & Robbins, T. W. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04143.x · Cited by 118 · see citing works
Ethanol induces impulsive-like responding in a delay-of-reward operant choice procedure: impulsivity predicts autoshaping
Tomie, A., Aguado, A. S., Pohorecky, L. A., & Benjamin, D. (1998) · Psychopharmacology · doi:10.1007/s002130050728 · Cited by 108 · see citing works
A DEMONSTRATION OF AUTO‐SHAPING WITH MONKEYS
Sidman, M., & Fletcher, F. G. (1968) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1968.11-307 · Cited by 104 · see citing works
Functional microcircuitry in the accumbens underlying drug addiction: insights from real-time signaling during behavior
Carelli, R. M., & Wightman, R. M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.10.001 · Cited by 103 · see citing works
Self-citation
Abstinence from Cocaine Self-Administration Heightens Neural Encoding of Goal-Directed Behaviors in the Accumbens
Hollander, J. A., & Carelli, R. M. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300748 · Cited by 94 · see citing works
Self-citation
Neuronal responses in prefrontal cortex and nucleus accumbens during heroin self-administration in freely moving rats
Chang, J.-Y., Zhang, L., Janak, P. H., & Woodward, D. J. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00012-7 · Cited by 83 · see citing works
Individual Differences in Pavlovian Autoshaping of Lever Pressing in Rats Predict Stress-Induced Corticosterone Release and Mesolimbic Levels of Monoamines
Tomie, A., Aguado, A., Pohorecky, L. A., & Benjamin, D. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00241-5 · Cited by 78 · see citing works
Phasic Firing Time Locked to Cocaine Self-Infusion and Locomotion: Dissociable Firing Patterns of Single Nucleus Accumbens Neurons in the Rat
Peoples, L. L., Gee, F., Bibi, R., & West, M. O. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07588.1998 · Cited by 76 · see citing works
AUTOSHAPING, RANDOM CONTROL, AND OMISSION TRAINING IN THE RAT1
Locurto, C., Terrace, H. S., & Gibbon, J. (1976) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1976.26-451 · Cited by 71 · see citing works
Pavlovian Conditioning With Ethanol: Sign‐Tracking (Autoshaping), Conditioned Incentive, and Ethanol Self‐Administration
Krank, M. D. (2003) · Alcoholism: Clinical and Experimental Research · doi:10.1097/01.alc.0000092060.09228.de · Cited by 65 · see citing works
A Comparison of Drug Conditioning and Craving for Alcohol and Cocaine
Newlin, D. B. (1992) · Recent developments in alcoholism · doi:10.1007/978-1-4899-1648-8_8 · Cited by 57 · see citing works
Differences Between Accumbens Core and Shell Neurons Exhibiting Phasic Firing Patterns Related to Drug-Seeking Behavior During a Discriminative-Stimulus Task
Ghitza, U. E., Fabbricatore, A. T., Prokopenko, V. F., & West, M. O. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00268.2004 · Cited by 54 · see citing works
Sign-tracking (autoshaping) in rats: A comparison of cocaine and food as unconditioned stimuli
Kearns, D. N., & Weiss, S. J. (2004) · Learning & Behavior · doi:10.3758/bf03196042 · Cited by 50 · see citing works
Sign tracking versus goal tracking in the sexual conditioning of male Japanese quail (Coturnix japonica).
Burns, M., & Domjan, M. P. (1996) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.22.3.297 · Cited by 45 · see citing works
Topography of spatially directed conditioned responding: Effects of context and trial duration.
Burns, M., & Domjan, M. P. (2001) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.27.3.269 · Cited by 39 · see citing works
Neuronal spike activity in rat nucleus accumbens during cocaine self-administration under different fixed-ratio schedules
Chang, J., Paris, J. M., Sawyer, S. F., Kirillov, A. B., & Woodward, D. J. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00144-3 · Cited by 38 · see citing works
Dissociation of locomotor and conditioned place preference responses following manipulation of GABA-A and AMPA receptors in ventral pallidum
Gong, W., Justice, J. B., & Neill, D. B. (1997) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(97)00084-5 · Cited by 36 · see citing works
AUTOSHAPING OF ETHANOL DRINKING: AN ANIMAL MODEL OF BINGE DRINKING
Tomie, A. (2002) · Alcohol and Alcoholism · doi:10.1093/alcalc/37.2.138 · Cited by 34 · see citing works
CS-UCS presentations and a lever: Human autoshaping.
Wilcove, W. G., & Miller, J. C. (1974) · Journal of Experimental Psychology · doi:10.1037/h0037388 · Cited by 32 · see citing works
Occupancy of brain nicotinic acetylcholine receptors by nicotine doses equivalent to those obtained when smoking a cigarette
Ding, Y., Volkow, N. D., Logan, J., Garza, V., Pappas, N. R., King, P. T., & Fowler, J. S. (2000) · Synapse · doi:10.1002/(sici)1098-2396(20000301)35:3 · Cited by 25 · see citing works
Nucleus accumbens neurons in the rat exhibit differential activity to conditioned reinforcers and primary reinforcers within a second‐order schedule of saccharin reinforcement
Wilson, D. I. G., & Bowman, E. M. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03747.x · Cited by 23 · see citing works
Higher magnitude accumbal phasic firing changes among core neurons exhibiting tonic firing increases during cocaine self-administration
Ghitza, U. E., Prokopenko, V. F., West, M. O., & Fabbricatore, A. T. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.026 · Cited by 22 · see citing works

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Balleine, B. W., & O'Doherty, J. P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.131 · Cited by 1,775 · see citing works
Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits
Salamone, J. D., Correa, M., Farrar, A., & Mingote, S. M. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0668-9 · Cited by 1,000 · see citing works
Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens
Day, J. J., Roitman, M. F., Wightman, R. M., & Carelli, R. M. (2007) · Nature Neuroscience · doi:10.1038/nn1923 · Cited by 710 · see citing works
Self-citation
Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction
Flagel, S. B., Akil, H., & Robinson, T. E. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.027 · Cited by 561 · see citing works
Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks
Yin, H. H., Ostlund, S. B., & Balleine, B. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06422.x · Cited by 416 · see citing works
Contributions of the striatum to learning, motivation, and performance: an associative account
Liljeholm, M., & O’Doherty, J. P. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.07.007 · Cited by 317 · see citing works
Which cue to "want?" Central amygdala opioid activation enhances and focuses incentive salience on a prepotent reward cue
Mahler, S. V., & Berridge, K. C. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3875-08.2009 · Cited by 223 · see citing works
Context, emotion, and the strategic pursuit of goals: interactions among multiple brain systems controlling motivated behavior
Gruber, A. J., & McDonald, R. J. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00050 · Cited by 173 · see citing works
The nucleus accumbens as a nexus between values and goals in goal-directed behavior: a review and a new hypothesis
Mannella, F., Gurney, K., & Baldassarre, G. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00135 · Cited by 166 · see citing works
Phasic Nucleus Accumbens Dopamine Encodes Risk-Based Decision-Making Behavior
Sugam, J. A., Day, J. J., Wightman, R. M., & Carelli, R. M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.09.029 · Cited by 142 · see citing works
Self-citation
Putting desire on a budget: dopamine and energy expenditure, reconciling reward and resources
Beeler, J. A., Frazier, C. R. M., & Zhuang, X. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00049 · Cited by 136 · see citing works
Dorsolateral caudate nucleus differentiates cocaine from natural reward-associated contextual cues
Liu, H.-S., Chefer, S., Lu, H., Guillem, K., Rea, W., Kurup, P., Yang, Y., Peoples, L., & Stein, E. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207531110 · Cited by 23 · see citing works

Effects of Inhibitory Signal on Criticality in Excitatory-Inhibitory Networks*
Wang, F., & Wang, S.-J. (2019) · Communications in Theoretical Physics · doi:10.1088/0253-6102/71/6/746 · Cited by 3 · see citing works
[Interaction of excitatory and inhibitory processes in the proposed inhibitory interneurons of the hippocampus].
Artemenko, D. P. (1980) · PubMed · Cited by 3 · see citing works
Difference in axon diameter and myelin thickness between excitatory and inhibitory callosally projecting axons in mice
Basu, K., Appukuttan, S., Manchanda, R., & Attila Gabor, S. I. K. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac329 · Cited by 28 · see citing works
What is the Source of the EEG?
Kirschstein, T., & Köhling, R. (2009) · Clinical EEG and Neuroscience · doi:10.1177/155005940904000305 · Cited by 206 · see citing works
Excitatory and Inhibitory Responses of the Ongoing Sympathetic Discharge in Single Renal Neurons to Liminal Stimulation of Aortic C-Fibres in the Rabbit
Lupa, K., Wójcik, G., Kruk, A., et al. (1999) · Archives of Physiology and Biochemistry · doi:10.1076/apab.107.2.113.4338

Authors: Day, J. J., Wheeler, R. A., Roitman, M. F., & Carelli, R. M.
Affiliations: University of North Carolina at Chapel Hill (US)
ORCID: Day, Jeremy J.
Roitman, Mitchell F.
Carelli, Regina M.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2006-03
Volume: 23
Issue: 5
Pages: 1341-1351
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/j.1460-9568.2006.04654.x
OpenAlex: W2170075413
Cited by: 140
References: 81
Citations by year: 2026: 3 · 2025: 6 · 2024: 3 · 2023: 8 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 13 · 2018: 7 · 2017: 6 · 2016: 10 · 2015: 6 · 2014: 9 · 2013: 7 · 2012: 9
FWCI: 2.90
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 7 d)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
Funders: National Institute on Drug Abuse (R01DA014339, DA 14339)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: nucleus accumbens, autoshaping, conditioned stimulus, phasic neuronal activity, excitatory and inhibitory neurons, sucrose reward, drug addiction, compulsive behavior, single-unit recording
MeSH terms: Action Potentials, Animals, Behavior, Animal, Conditioning, Classical, Electrophysiology, Humans, Male, Neurons, Nucleus Accumbens, Sucrose, Rats, Sprague-Dawley, Substance-Related Disorders, Rats

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Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm

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