Developmental disruption of gamma-aminobutyric acid function in the medial prefrontal cortex by noncontingent cocaine exposure during early adolescence

Cass, Daryn K.; Thomases, Daniel R.; Caballero, Adriana; Tseng, Kuei Y.

doi:10.1016/j.biopsych.2013.02.021

Cited by 63Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Developmental disruption of gamma-aminobutyric acid function in the medial prefrontal cortex by noncontingent cocaine exposure during early adolescence

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Cass, Daryn K., Thomases, Daniel R., Caballero, Adriana, Tseng, Kuei Y.·2013·Biological Psychiatry

DOI 10.1016/j.biopsych.2013.02.021PMC PMC3722277

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Abstract

Background Drug experimentation during adolescence is associated with increased risk of drug addiction relative to any other age group. To further understand the neurobiology underlying such liability, we investigate how early adolescent cocaine experience impacts medial prefrontal cortex (mPFC) network function in adulthood.Methods A noncontingent administration paradigm was used to assess the impact of early adolescent cocaine treatment (rats; postnatal days [PD] 35-40) on the overall inhibitory regulation of mPFC activity in adulthood (PD 65-75) by means of histochemical and in vivo electrophysiological measures combined with pharmacologic manipulations.Results Cocaine exposure during early adolescence yields a distinctive hypermetabolic prefrontal cortex state that was not observed in adult-treated rats (PD 75-80). Local field potential recordings revealed that early adolescent cocaine exposure is associated with an attenuation of mPFC gamma-aminobutyric acid (GABA)ergic inhibition evoked by ventral hippocampal stimulation at beta and gamma frequencies that endures throughout adulthood. Such cocaine-induced mPFC disinhibition was not observed in adult-exposed animals. Furthermore, the normal developmental upregulation of parvalbumin immunoreactivity observed in the mPFC from PD 35 to PD 65 is lacking following early adolescent cocaine treatment.Conclusions Our data indicate that repeated cocaine exposure during early adolescence can elicit a state of mPFC disinhibition resulting from a functional impairment of the local prefrontal GABAergic network that endures through adulthood. A lack of acquisition of prefrontal GABAergic function during adolescence could trigger long-term deficits in the mPFC that may increase the susceptibility for the onset of substance abuse and related psychiatric disorders.

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In rodents, cocaine exposure in adolescence, but not adulthood, produces a long-lasting attenuation of medial PFC GABAergic activity and parvalbumin cell expression that remains evident in adulthood.
“In rodents, cocaine exposure in adolescence, but not adulthood, produces a long-lasting attenuation of medial PFC (mPFC) GABAergic activity and parvalbumin cell expression that remains evident in adulthood (Cass et al., 2013).”
From Sensitive periods of substance abuse: Early risk for the transition to dependence (2017) · cites this paper as Cass et al., 2013

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Dynamic mapping of human cortical development during childhood through early adulthood
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. F., Herman, D. H., Clasen, L. S., Toga, A. W., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402680101 · Cited by 5,604 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Handbook of Chemical Neuroanatomy
Stern, C. D. (1986) · Neurochemistry International · doi:10.1016/0197-0186(86)90021-5 · Cited by 4,159 · see citing works
J Neuropsychiatry Clin Neurosci
Yudofsky, S. C., & Hales, R. E. (1992) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.4.4.359 · Cited by 3,818 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Drug Addiction and Its Underlying Neurobiological Basis: Neuroimaging Evidence for the Involvement of the Frontal Cortex
Goldstein, R. Z., & Volkow, N. D. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.10.1642 · Cited by 2,667 · see citing works
Neurobiology of emotion perception I: the neural basis of normal emotion perception
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00168-9 · Cited by 2,173 · cited 1× · see citing works
“While ventral hippocampal inputs to the mPFC play a critical role in the control of working memory, decision making and impulsive behavior (52, 53), afferent information from the basolateral amygdala is required for the integration of emotionally salient information (54, 55).”
Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability
Chambers, R. A., Taylor, J. R., & Potenza, M. N. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.6.1041 · Cited by 1,719 · cited 6× · see citing works
“0001; treatment x age interaction F(2,42)=5.”
Influential
A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory
Braver, T. S., Cohen, J. D., Nystrom, L. E., Jonides, J., Smith, E. E., & Noll, D. C. (1997) · NeuroImage · doi:10.1006/nimg.1996.0247 · Cited by 1,694 · see citing works
Limbic Activation During Cue-Induced Cocaine Craving
Childress, A. R., Mozley, P. D., McElgin, W., Fitzgerald, J., Reivich, M., & O’Brien, C. P. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.1.11 · Cited by 1,513 · see citing works
Structural and functional brain development and its relation to cognitive development
Casey, B. J., Giedd, J. N., & Thomas, K. M. (2000) · Biological Psychology · doi:10.1016/s0301-0511(00)00058-2 · Cited by 1,506 · see citing works
Trajectories of brain development: point of vulnerability or window of opportunity?
Andersen, S. L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00005-8 · Cited by 1,503 · cited 10× · see citing works
“At 20Hz, a shift from the transient attenuation to sustained facilitation of the evoked LFP response was observed in the mPFC after local administration of picrotoxin (n=5 per group; main treatment effect F(1,40)=51.”
Influential
Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior
McFarland, K., & Kalivas, P. W. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08655.2001 · Cited by 905 · cited 7× · see citing works
“(B) Additional recordings revealed that early adolescent cocaine-induced attenuation of mPFC LFP inhibition at 40Hz is long-lasting and detectable at PD105-115 (n=6 per group; main pulse number effect F(9,100)=44.”
Influential
Physiological Dysfunction of the Dorsolateral Prefrontal Cortex in Schizophrenia Revisited
Callicott, J. H. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.11.1078 · Cited by 810 · see citing works
Physiological characteristics of capacity constraints in working memory as revealed by functional MRI
Callicott, J. H. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.1.20 · Cited by 771 · see citing works
Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes
Belforte, J. E., Zsiros, V., Sklar, E. R., Jiang, Z., Yu, G., Li, Y., Quinlan, E. M., & Nakazawa, K. (2010) · Nature Neuroscience · doi:10.1038/nn.2447 · Cited by 752 · see citing works
Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay
Floresco, S., Seamans, J. K., & Phillips, A. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-05-01880.1997 · Cited by 734 · cited 1× · see citing works
“While ventral hippocampal inputs to the mPFC play a critical role in the control of working memory, decision making and impulsive behavior (52, 53), afferent information from the basolateral amygdala is required for the integration of emotionally salient information (54, 55).”
A mechanism for generation of long-range synchronous fast oscillations in the cortex
Traub, R. D., Whittington, M. A., Stanford, I. M., & Jefferys, J. G. R. (1996) · Nature · doi:10.1038/383621a0 · Cited by 701 · cited 2× · see citing works
“7), whereas an overall downregulation of CO-I staining was observed in adult-treated animals (n=10–12 per group; main age effect F(1,66)=26.”
Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings
Manoach, D. S. (2003) · Schizophrenia Research · doi:10.1016/s0920-9964(02)00294-3 · Cited by 681 · cited 2× · see citing works
“However, hypofrontality is currently perceived as a state of functional impairment characterized by a failure of the PFC to support behavior (46, 47).”
Impulsivity, frontal lobes and risk for addiction
Crews, F. T., & Boettiger, C. A. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.018 · Cited by 679 · see citing works
Normalization
Rinaldi, C. (2014) · Encyclopedia of Social Deviance · doi:10.4135/9781483340470.n189 · Cited by 636 · see citing works
Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates
Berger, B., Gaspar, P., & Verney, C. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90179-x · Cited by 588 · cited 1× · see citing works
“Together with the distinct rostro-caudal gradient of cortical dopamine innervation (74, 75), we hypothesize that the rostral level of the frontal cortex is highly susceptible to the effects of cocaine or other psychostimulants when administered during adolescence.”
Ketamine-Induced Loss of Phenotype of Fast-Spiking Interneurons Is Mediated by NADPH-Oxidase
Behrens, M. M., Ali, S. S., Dao, D. N., Lucero, J., Shekhtman, G., Quick, K. L., & Dugan, L. L. (2007) · Science · doi:10.1126/science.1148045 · Cited by 585 · cited 1× · see citing works
“Since the functional profile of PV-positive interneurons and the PV expression level are tightly correlated (34, 58), the reduced PV immunoreactivity observed in the mPFC after early adolescent cocaine could be therefore attributable to a developmental disruption of PV interneuron maturation and function that endures…”
Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task
Bolla, K. I., Eldreth, D. A., London, E. D., Kiehl, K. A., Mouratidis, M., Contoreggi, C. S., Matochik, J. A., Kurian, V., Cadet, J. L., Kimes, A. S., et al. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00113-7 · Cited by 578 · cited 7× · see citing works
“0005; treatment x pulse number interaction F(4,40)=3.”
Influential
Structural Brain Imaging Evidence for Multiple Pathological Processes at Different Stages of Brain Development in Schizophrenia
Pantelis, C. (2005) · Schizophrenia Bulletin · doi:10.1093/schbul/sbi034 · Cited by 573 · see citing works
Limbic and Motor Circuitry Underlying Footshock-Induced Reinstatement of Cocaine-Seeking Behavior
McFarland, K., Davidge, S. B., Lapish, C. C., & Kalivas, P. W. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4177-03.2004 · Cited by 524 · cited 1× · see citing works
“Interestingly, stress-induced relapse has been shown to be, at least in part, dependent upon the PFC (10, 68, 69).”
GABAergic interneuron origin of schizophrenia pathophysiology
Nakazawa, K., Zsiros, V., Jiang, Z., Nakao, K., Kolata, S., Zhang, S., & Belforte, J. E. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.022 · Cited by 498 · cited 3× · see citing works
“Among the three distinctive subtypes of interneurons expressing Ca++-binding proteins in the PFC, a downregulation of the parvalbumin (PV)-positive fast-spiking interneuron function has been associated with the development of prefrontal disinhibition in animal models (21, 30).”
A Loss of Parvalbumin-Containing Interneurons Is Associated with Diminished Oscillatory Activity in an Animal Model of Schizophrenia
Lodge, D. J., Behrens, M. M., & Grace, A. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5419-08.2009 · Cited by 488 · see citing works
Changes in brain glucose metabolism in cocaine dependence and withdrawal
Volkow, N. D., Fowler, J. S., Wolf, A. P., Hitzemann, R., Dewey, S. L., Bendriem, B., Alpert, R., & Hoff, A. L. (1991) · American Journal of Psychiatry · doi:10.1176/ajp.148.5.621 · Cited by 447 · see citing works
A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats
Capriles, N., Rodaros, D., Sorge, R. E., & Stewart, J. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1283-z · Cited by 414 · cited 1× · see citing works
“Interestingly, stress-induced relapse has been shown to be, at least in part, dependent upon the PFC (10, 68, 69).”
Long‐Term frontal brain metabolic changes in cocaine abusers
Volkow, N. D., HITZEMANN, R. J., Wang, G., Fowler, J. S., Wolf, A. P., Dewey, S. L., & Handlesman, L. (1992) · Synapse · doi:10.1002/syn.890110303 · Cited by 411 · see citing works
Destruction and Creation of Spatial Tuning by Disinhibition: GABA<sub>A</sub>Blockade of Prefrontal Cortical Neurons Engaged by Working Memory
Rao, S. G., Williams, G. V., & Goldman-Rakic, P. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00485.2000 · Cited by 407 · cited 1× · see citing works
“Among the different subsets of GABAergic interneurons in the PFC, the parvalbumin (PV)-positive/fast-spiking cells play an important role in determining the timing and spatial selectivity of pyramidal cell firing (18).”
Essential Role of D1 But Not D2 Receptors in the NMDA Receptor-Dependent Long-Term Potentiation at Hippocampal-Prefrontal Cortex SynapsesIn Vivo
Gurden, H., Takita, M., & Jay, T. M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-22-j0003.2000 · Cited by 366 · cited 1× · see citing works
“It is well known that changes in synaptic plasticity within the ventral hippocampal-prefrontal pathway can be assessed in vivo by means of local field potentials (29).”
Cerebral Blood Flow in Chronic Cocaine Users: A Study with Positron Emission Tomography
Volkow, N. D., Mullani, N. A., Gould, K. L., Adler, S., & Krajewski, K. J. (1988) · The British Journal of Psychiatry · doi:10.1192/bjp.152.5.641 · Cited by 365 · see citing works
Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models
Laviola, G., Adriani, W., Terranova, M. L., & Gerra, G. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00032-9 · Cited by 345 · cited 10× · see citing works
“0005; treatment x pulse number interaction F(4,40)=3.”
Influential
Dopamine Modulation of Prefrontal Cortical Interneurons Changes during Adolescence
Tseng, K.-Y., & O'Donnell, P. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl034 · Cited by 339 · cited 2× · see citing works
“Thus, the acquisition of an increased prefrontal GABAergic function during the normal adolescent period (19, 20) is thought to be associated with the maturation of cognitive abilities such as working memory, decision making and impulse control (21, 22).”
Self-citation
The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia
Tseng, K. Y., Chambers, R. A., & Lipska, B. K. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.039 · Cited by 336 · cited 1× · see citing works
“At the cellular level, the maturation of PFC activity during adolescence is dependent on the remodeling of local inhibitory circuits by the influence of glutamatergic inputs from the ventral hippocampus and the recruitment of dopamine facilitatory action on GABAergic interneurons (16, 17).”
Self-citation
Prefrontal Cortical Dysfunction in Abstinent Cocaine Abusers
Bolla, K. I., Ernst, M., Kiehl, K. A., Mouratidis, M., Eldreth, D. A., Contoreggi, C. S., Matochik, J. A., Kurian, V., Cadet, J. L., Kimes, A. S., et al. (2004) · Journal of Neuropsychiatry · doi:10.1176/jnp.16.4.456 · Cited by 258 · see citing works
Dose-Related Neurobehavioral Effects of Chronic Cocaine Use
Bolla, K. I., Rothman, R. B., & Cadet, J. L. (1999) · Journal of Neuropsychiatry · doi:10.1176/jnp.11.3.361 · Cited by 214 · see citing works
Convergence and Interaction of Hippocampal and Amygdalar Projections within the Prefrontal Cortex in the Rat
Ishikawa, A., & Nakamura, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09987.2003 · Cited by 185 · cited 1× · see citing works
“While ventral hippocampal inputs to the mPFC play a critical role in the control of working memory, decision making and impulsive behavior (52, 53), afferent information from the basolateral amygdala is required for the integration of emotionally salient information (54, 55).”
Motivated attention to cocaine and emotional cues in abstinent and current cocaine users - an ERP study
Dunning, J. P., Parvaz, M. A., Hajcak, G., Maloney, T., Nelly Alia-klein, A., Woicik, P. A., Telang, F., Wang, G., Volkow, N. D., & Goldstein, R. Z. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07663.x · Cited by 182 · see citing works
Differential developmental trajectories for CB1 cannabinoid receptor expression in limbic/associative and sensorimotor cortical areas
Heng, L., Beverley, J. A., Steiner, H., & Tseng, K. Y. (2010) · Synapse · doi:10.1002/syn.20844 · Cited by 180 · cited 1× · see citing works
“Since this effect was not observed in adult-treated animals, it is likely that the restricted pattern of alterations resulting from early adolescent exposure to cocaine is due to the shared developmental trajectory of inhibitory elements in the rostral regions of the frontal cortex (31, 73).”
Self-citation
Reducing Prefrontal Gamma-Aminobutyric Acid Activity Induces Cognitive, Behavioral, and Dopaminergic Abnormalities That Resemble Schizophrenia
Enomoto, T., Tse, M. T., & Floresco, S. B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.038 · Cited by 179 · see citing works
Differential regulation of parvalbumin and calretinin interneurons in the prefrontal cortex during adolescence
Caballero, A., Flores-Barrera, E., Cass, D. K., & Tseng, K. Y. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0508-8 · Cited by 178 · see citing works
Self-citation
The Development of Neural Synchrony and Large-Scale Cortical Networks During Adolescence: Relevance for the Pathophysiology of Schizophrenia and Neurodevelopmental Hypothesis
Uhlhaas, P. J., & Singer, W. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr034 · Cited by 176 · cited 1× · see citing works
“Thus, the acquisition of an increased prefrontal GABAergic function during the normal adolescent period (19, 20) is thought to be associated with the maturation of cognitive abilities such as working memory, decision making and impulse control (21, 22).”
Stimulants and the developing brain
Andersen, S. L. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.03.009 · Cited by 168 · see citing works
More Is Less: A Disinhibited Prefrontal Cortex Impairs Cognitive Flexibility
Gruber, A. J., Calhoon, G. G., Shusterman, I., Schoenbaum, G., Roesch, M. R., & O'Donnell, P. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-10.2010 · Cited by 160 · see citing works
Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex
Woo, T.-U., Pucak, M. L., Kye, C. H., Matus, C. V., & Lewis, D. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00059-6 · Cited by 157 · see citing works
Adolescent Onset of Cortical Disinhibition in Schizophrenia: Insights From Animal Models
O'Donnell, P. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr028 · Cited by 145 · cited 3× · see citing works
“Among the three distinctive subtypes of interneurons expressing Ca++-binding proteins in the PFC, a downregulation of the parvalbumin (PV)-positive fast-spiking interneuron function has been associated with the development of prefrontal disinhibition in animal models (21, 30).”
A Neonatal Ventral Hippocampal Lesion Causes Functional Deficits in Adult Prefrontal Cortical Interneurons
Tseng, K. Y., Lewis, B. L., Hashimoto, T., Sesack, S. R., Kloc, M., Lewis, D. A., & O'Donnell, P. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4166-08.2008 · Cited by 144 · cited 1× · see citing works
“At the cellular level, the maturation of PFC activity during adolescence is dependent on the remodeling of local inhibitory circuits by the influence of glutamatergic inputs from the ventral hippocampus and the recruitment of dopamine facilitatory action on GABAergic interneurons (16, 17).”
Self-citation
D <sub>2</sub> dopamine receptors recruit a GABA component for their attenuation of excitatory synaptic transmission in the adult rat prefrontal cortex
Tseng, K. Y., & O'Donnell, P. (2007) · Synapse · doi:10.1002/syn.20432 · Cited by 141 · see citing works
Self-citation
Uncoupling Cognitive Workload and Prefrontal Cortical Physiology: A PET rCBF Study
Goldberg, T. E., Berman, K. F., Fleming, K., Ostrem, J. L., Horn, J. D. V., Esposito, G., Mattay, V. S., Gold, J. M., & Weinberger, D. R. (1998) · NeuroImage · doi:10.1006/nimg.1998.0338 · Cited by 140 · see citing works
β and γ Frequency Synchronization by Dendritic GABAergic Synapses and Gap Junctions in a Network of Cortical Interneurons
Szabadics, J., Lörincz, A., & Tamás, G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05824.2001 · Cited by 134 · see citing works
Elevated BDNF after Cocaine Withdrawal Facilitates LTP in Medial Prefrontal Cortex by Suppressing GABA Inhibition
Lü, H., Cheng, P., Lim, B. K., Khoshnevisrad, N., & Poo, M. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.012 · Cited by 134 · cited 1× · see citing works
“These findings are consistent with a recent study conducted in PFC brain slices showing that drug withdrawal from cocaine-sensitized juvenile rats favors the expression of activity-induced glutamatergic LTP onto pyramidal neurons, an effect thought to be triggered by a downregulation of local GABA-A receptormediated i…”
Functional characteristics of parvalbumin‐ and cholecystokinin‐expressing basket cells
Bartos, M., & Elgueta, C. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226175 · Cited by 127 · cited 1× · see citing works
“PV-containing cells, often referred as fast-spiking GABAergic interneurons, are functionally positioned to exert fast, stable and timed feedforward inhibition onto pyramidal output cells in respond to highfrequency excitatory inputs (see review by (59)).”
How the 'slow' Ca2+ buffer parvalbumin affects transmitter release in nanodomain-coupling regimes
Eggermann, E., & Jonas, P. (2012) · Nature Neuroscience · doi:10.1038/nn.3002 · Cited by 119 · cited 2× · see citing works
“Since the functional profile of PV-positive interneurons and the PV expression level are tightly correlated (34, 58), the reduced PV immunoreactivity observed in the mPFC after early adolescent cocaine could be therefore attributable to a developmental disruption of PV interneuron maturation and function that endures…”
Understanding the neurobiological consequences of early exposure to psychotropic drugs: linking behavior with molecules
Carlezon, W. A., & Konradi, C. L. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.021 · Cited by 111 · see citing works
Delayed response deficits produced by local injection of bicuculline into the dorsolateral prefrontal cortex in Japanese macaque monkeys
Sawaguchi, T., Matsumura, M., & Kubota, K. (1989) · Experimental Brain Research · doi:10.1007/bf00249897 · Cited by 109 · see citing works
Hippocampal-Prefrontal Cortical Circuit Mediates Inhibitory Response Control in the Rat
Chudasama, Y., Doobay, V. M., & Liu, Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1463-12.2012 · Cited by 97 · cited 1× · see citing works
“While ventral hippocampal inputs to the mPFC play a critical role in the control of working memory, decision making and impulsive behavior (52, 53), afferent information from the basolateral amygdala is required for the integration of emotionally salient information (54, 55).”
Prenatal cocaine exposure produces consistent developmental alterations in dopamine-rich regions of the cerebral cortex
Stanwood, G. D., Washington, R. A., Shumsky, J. S., & Levitt, P. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00256-1 · Cited by 94 · cited 1× · see citing works
“, mPFC) have been repeatedly observed following prenatal cocaine exposure (56, 57).”
Periadolescent Exposure to the NMDA Receptor Antagonist MK-801 Impairs the Functional Maturation of Local GABAergic Circuits in the Adult Prefrontal Cortex
Thomases, D. R., Cass, D. K., & Tseng, K. Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4147-12.2013 · Cited by 89 · cited 4× · see citing works
“Consistent with our recent study (26), a proper functioning of local GABA-A receptor-mediated transmission is required in the normal adult mPFC for sustaining the characteristic frequency-dependent inhibition of prefrontal LFP responses to ventral hippocampal stimulation at 20Hz and 40Hz.”
InfluentialSelf-citation
Adolescents are more vulnerable to cocaine addiction: behavioral and electrophysiological evidence
Wong, W. C., Ford, K. A., Pagels, N. E., McCutcheon, J. E., & Marinelli, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1371-12.2013 · Cited by 87 · cited 1× · see citing works
“For example, a recent study by the Marinelli group (67) using a self-administration paradigm demonstrated that adolescent onset of cocaine use produces greater stress-induced relapse after prolonged withdrawal, compared with adult-onset of cocaine use.”
Parallel studies of cocaine-related neural and cognitive impairment in humans and monkeys
Beveridge, T. J. R., Gill, K. E., Hanlon, C. A., & Porrino, L. J. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0102 · Cited by 86 · see citing works
A key mechanism underlying sensory experience-dependent maturation of neocortical GABAergic circuits in vivo
Jiao, Y., Zhang, Z., Zhang, C., Wang, X., Sakata, K., Lu, B., & Sun, Q. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105296108 · Cited by 84 · see citing works
Adolescent Development of Forebrain Stimulant Responsiveness: Insights from Animal Studies
LESLIE, F. M., LOUGHLIN, S. E., WANG, R., PEREZ, L., LOTFIPOUR, S., & BELLUZZIA, J. D. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.018 · Cited by 81 · cited 1× · see citing works
“Similar impairments in prefrontal-dependent executive functions have been observed after long-term exposure to psychostimulants during adolescence (2, 3, 45).”
NEURONAL SUBSTRATES OF RELAPSE TO COCAINE-SEEKING BEHAVIOR: ROLE OF PREFRONTAL CORTEX
Rebec, G. V., & Sun, W. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.105-04 · Cited by 76 · cited 1× · see citing works
“Interestingly, stress-induced relapse has been shown to be, at least in part, dependent upon the PFC (10, 68, 69).”
Identification of a Sensitive Period of Prenatal Cocaine Exposure that Alters the Development of the Anterior Cingulate Cortex
Stanwood, G. D. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.5.430 · Cited by 75 · see citing works
Decision-Making Deficits Linked to Real-life Social Dysfunction in Crack Cocaine-Dependent Individuals
Cunha, P. J., Bechara, A., de Andrade, A. G., & Nicastri, S. (2010) · American Journal on Addictions · doi:10.1111/j.1521-0391.2010.00097.x · Cited by 70 · cited 4× · see citing works
“0001; treatment x age interaction F(2,42)=5.”
Influential
A pattern of perseveration in cocaine addiction may reveal neurocognitive processes implicit in the Wisconsin Card Sorting Test
Woicik, P. A., Urban, C., Nelly Alia-klein, A., Henry, A., Maloney, T., Telang, F., Wang, G., Volkow, N. D., & Goldstein, R. Z. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2011.02.037 · Cited by 69 · see citing works
Delayed response deficit in monkeys by locally disturbed prefrontal neuronal activity by bicuculline
Sawaguchi, T., MATSUMURA, M., & KUBOTA, K. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90023-x · Cited by 63 · see citing works
Subnuclear localization of FOS‐like immunoreactivity in the parabrachial nucleus after orofacial nociceptive stimulation of the awake rat
Hermanson, O., & Blomqvist, A. (1997) · The Journal of comparative neurology · doi:10.1002/(sici)1096-9861(19971013)387:1 · Cited by 61 · see citing works
Inhibition of Striatal Soluble Guanylyl Cyclase-cGMP Signaling Reverses Basal Ganglia Dysfunction and Akinesia in Experimental Parkinsonism
Tseng, K. Y., Caballero, A. C., Dec, A. M., Cass, D. K., Simak, N., Sunu, E., Park, M. J., Blume, S. R., Sammut, S., Park, D. J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027187 · Cited by 46 · cited 2× · see citing works
“, Roanoke, VA) secured to the mPFC recording electrode, as previously described (28).”
Self-citation
Altered Prefrontal Cortical Metabolic Response to Mesocortical Activation in Adult Animals with a Neonatal Ventral Hippocampal Lesion
Tseng, K. Y., Amin, F., Lewis, B. L., & O’Donnell, P. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.030 · Cited by 43 · cited 1× · see citing works
“Brain metabolic activity was determined by means of cytochrome oxidase staining using a previously reported protocol (Supplement 1) (27, 28).”
Self-citation
Altered Dopamine Modulation of Inhibition in the Prefrontal Cortex of Cocaine-Sensitized Rats
Kroener, S., & Lavı́n, A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.107 · Cited by 41 · cited 9× · see citing works
“0005; treatment x pulse number interaction F(4,60)=3.”
Influential
Prenatal exposure to cocaine selectively disrupts the development of parvalbumin containing local circuit neurons in the medial prefrontal cortex of the rat
Morrow, B. A., Elsworth, J. D., & Roth, R. H. (2005) · Synapse · doi:10.1002/syn.20121 · Cited by 21 · cited 1× · see citing works
“, mPFC) have been repeatedly observed following prenatal cocaine exposure (56, 57).”

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Sensitive periods of substance abuse: Early risk for the transition to dependence
Jordan, C. J., & Andersen, S. L. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2016.10.004 · Cited by 455 · see citing works
Mechanisms contributing to prefrontal cortex maturation during adolescence
Caballero, A., Granberg, R., & Tseng, K. Y. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.013 · Cited by 357 · see citing works
“As reviewed here, susceptibility to developmental insults is certainly high during the periadolescent transition period, an impact that is likely to disrupt PFC maturation and functioning through adulthood (Cass et al., 2014; Cass et al., 2013; Thomases et al., 2014; Thomases et al., 2013).”
Self-citation
GABAergic Function as a Limiting Factor for Prefrontal Maturation during Adolescence
Caballero, A. C., & Tseng, K. Y. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.04.010 · Cited by 178 · see citing works
Self-citation
CB1 cannabinoid receptor stimulation during adolescence impairs the maturation of GABA function in the adult rat prefrontal cortex
Cass, D. K., Flores-Barrera, E., Thomases, D. R., Vital, W. F., Caballero, A. C., & Tseng, K. Y. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.14 · Cited by 181 · see citing works
Self-citation
Consequences of adolescent use of alcohol and other drugs: Studies using rodent models
SPEAR, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.026 · Cited by 154 · see citing works
“…gross structural alterations (Wheeler et al, 2013), such exposure has been reported to induce long-lasting increases in metabolic activity in the PFC, a “hypermetabolic PFC” than contrasts with the hypometabolic state reported after repeated cocaine exposure in adulthood (Cass et al, 2013).”
BackgroundInfluential
Adolescent drug exposure: A review of evidence for the development of persistent changes in brain function
Salmanzadeh, H., Ahmadi‐Soleimani, S. M., Pachenari, N., Azadi, M., Halliwell, R. F., Rubino, T., & Azizi, H. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.01.007 · Cited by 146 · see citing works
Developmental regulation of excitatory-inhibitory synaptic balance in the prefrontal cortex during adolescence
Caballero, A., Orozco, A., & Tseng, K. Y. (2021) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2021.02.008 · Cited by 83 · see citing works
Self-citation
Late Adolescent Expression of GluN2B Transmission in the Prefrontal Cortex Is Input-Specific and Requires Postsynaptic Protein Kinase A and D1 Dopamine Receptor Signaling
Flores-Barrera, E., Thomases, D. R., Heng, L., Cass, D. K., Caballero, A. C., & Tseng, K. Y. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.033 · Cited by 87 · see citing works
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Emergence of GABAergic-dependent regulation of input-specific plasticity in the adult rat prefrontal cortex during adolescence
Caballero, A. C., Thomases, D. R., Flores-Barrera, E., Cass, D. K., & Tseng, K. Y. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3216-4 · Cited by 82 · see citing works
Self-citation
Downregulation of parvalbumin expression in the prefrontal cortex during adolescence causes enduring prefrontal disinhibition in adulthood
Caballero, A., Flores-Barrera, E., Thomases, D. R., & Tseng, K. Y. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0709-9 · Cited by 77 · see citing works
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Hypervulnerability of the adolescent prefrontal cortex to nutritional stress via reelin deficiency
Labouesse, M. A., Lassalle, O., Richetto, J., Iafrati, J., Weber‐Stadlbauer, U., Notter, T., Gschwind, T., Pujadas, L., Soriano, E., Reichelt, A. C., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.193 · Cited by 75 · see citing works
Stress, sensitive periods, and substance abuse
Andersen, S. L. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100140 · Cited by 92 · see citing works
“In terms of drug abuse, non-contingent cocaine exposure in adolescent, but not adult, rodents produced an enduring attenuation of medial prefrontal GABAergic activity and PV cell expression, which is postulated to increase the risk of SUD long-term (Cass et al., 2013).”
Background
Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner
Reynolds, L. M., Makowski, C., Yogendran, S., Kießling, S., Cermakian, N., & Flores, C. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.287 · Cited by 60 · see citing works
“In parallel to these changes in dopamine circuitry, local mPFC neurons shift towards a mature state of responsiveness to the modulatory effects of dopamine (Spear, 2000; Tseng and O’Donnell, 2007; O’Donnell, 2011; Cass et al, 2013).”
Background
Impact of Environmental Enrichment on Perineuronal Nets in the Prefrontal Cortex following Early and Late Abstinence from Sucrose Self-Administration in Rats
Slaker, M. L., Barnes, J., Sorg, B. A., & Grimm, J. W. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168256 · Cited by 57 · see citing works
Genetic Architecture and Molecular Neuropathology of Human Cocaine Addiction
Huggett, S. B., & Stallings, M. C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2879-19.2020 · Cited by 47 · see citing works
“PFC GABAergic signaling is sparsely studied in rodent models of cocaine use, but some evidence suggests that GABA regulates prefrontal disinhibition (Cass et al., 2013).”
Background
Vagal nerve stimulation blocks interleukin 6-dependent synaptic hyperexcitability induced by lipopolysaccharide-induced acute stress in the rodent prefrontal cortex
Garcia-Oscos, F., Peña, D., Housini, M., Cheng, D., Lopez, D., Borland, M. S., Salgado-Delgado, R., Salgado, H., D’Mello, S., Kilgard, M. P., et al. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.07.020 · Cited by 43 · see citing works
Stress rapidly dysregulates the glutamatergic synapse in the prefrontal cortex of cocaine-withdrawn adolescent rats
Caffino, L., Calabrese, F., Giannotti, G., Barbon, A., Verheij, M. M. M., Racagni, G., & Fumagalli, F. (2013) · Addiction Biology · doi:10.1111/adb.12089 · Cited by 37 · see citing works
“We then shifted our attention to the GABA network, as it has recently been shown that non-contingent cocaine exposure during adolescence disrupts GABA functions in the mPFC (Cass et al. 2013).”
Background
Metabolic alterations in the anterior cingulate cortex and related cognitive deficits in late adolescent methamphetamine users
Kim, J. E., Kim, G. H., Hwang, J., Kim, J., Renshaw, P. F., Yurgelun-Todd, D. A., Kim, B., Kang, I., Jeon, S.-R., Ma, J., et al. (2016) · Addiction Biology · doi:10.1111/adb.12473 · Cited by 36 · see citing works
“Furthermore, converging evidence from preclinical studies suggests that exposure to psychostimulants during the critical period of prefrontal development may induce long-lasting changes in the brain that may contribute to the progression of addictive behaviors into adulthood (Cass et al. 2013).”
Influential
Preferential Disruption of Prefrontal GABAergic Function by Nanomolar Concentrations of the α7nACh Negative Modulator Kynurenic Acid
Flores-Barrera, E., Thomases, D. R., Cass, D. K., Bhandari, A., Schwarcz, R. M., Bruno, J. P., & Tseng, K. Y. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0932-17.2017 · Cited by 30 · see citing works
“Accordingly, the frequency-dependent LFP disinhibition elicited by PFC infusion of KYNA is indistinguishable from that induced by the GABAAR antagonist picrotoxin (Cass et al., 2013; Thomases et al., 2013).”
BackgroundMethodSelf-citation
Animal Models of Maladaptive Traits: Disorders in Sensorimotor Gating and Attentional Quantifiable Responses as Possible Endophenotypes
Vargas, J. P., Díaz, E., Portavella, M., & López, J. C. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00206 · Cited by 28 · see citing works
Dopamine D1-D2 Receptor Heteromer Regulates Signaling Cascades Involved in Addiction: Potential Relevance to Adolescent Drug Susceptibility
Perreault, M. L., O’Dowd, B. F., & George, S. R. (2014) · Developmental Neuroscience · doi:10.1159/000360158 · Cited by 28 · see citing works
The transcription factor Npas4 contributes to adolescent development of prefrontal inhibitory circuits, and to cognitive and emotional functions: Implications for neuropsychiatric disorders
Shepard, R. M., Heslin, K. A., & Coutellier, L. D. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.12.012 · Cited by 27 · see citing works
“These changes contribute to the acquisition of inhibitory control through a gain of local GABAergic function (Thomases et al., 2013; Cass et al., 2013).”
Background
Proteomic and Metabolomic Analyses of Leaf from Clematis terniflora DC. Exposed to High-Level Ultraviolet-B Irradiation with Dark Treatment
Yang, B., Wang, X., Gao, C., Meng, C., Guan, Q., Tian, J., & Komatsu, S. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00206 · Cited by 28 · see citing works
Adolescent cocaine exposure enhances the GABAergic transmission in the prelimbic cortex of adult mice
Shi, P., Nie, J., Liu, H., Li, Y., Lu, X., Shen, X., Ge, F., Yuan, T., & Guan, X. (2019) · The FASEB Journal · doi:10.1096/fj.201802192rr · Cited by 28 · see citing works
“animals, repeated exposure to amphetamine from P27 to P45 suppress IPSCs of mPFC in mice at the young adult stage (36), whereas cocaine exposure from P35 to P40 disrupts GABAergic network in mPFC, which subsequently accounts for the disinhibition status for mPFC in adult rats (37).”
Background
MK-801 Exposure during Adolescence Elicits Enduring Disruption of Prefrontal E–I Balance and Its Control of Fear Extinction Behavior
Flores-Barrera, E., Thomases, D. R., & Tseng, K. Y. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0581-20.2020 · Cited by 26 · see citing works
“I imbalance observed in the PFC of adolescent MK-801-treated rats could arise from a deficient recruitment of local GABAergic function by excitatory inputs during adolescence (Cass et al., 2013; Thomases et al. 2013, 2014; Caballero et al., 2014b).”
BackgroundSelf-citation
Long-term effects of chronic cocaine exposure throughout adolescence on anxiety and stress responsivity in a Wistar rat model
Alves, C. J., Magalhães, A., Melo, P., de Sousa, L., Tavares, M. A., Monteiro, P. R. R., & Summavielle, T. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.008 · Cited by 26 · see citing works
“Compromised medial prefrontal cortex function predicts the development of impulsive behavior and impaired decision-making, which are behavioral traits associated with increased susceptibility for substance abuse (Cass et al., 2013; Kuhn et al., 2013).”
BackgroundInfluential
Exposure of adolescent mice to 3,4‐methylenedioxypyrovalerone increases the psychostimulant, rewarding and reinforcing effects of cocaine in adulthood
López‐Arnau, R., Luján, M. Á., Duart-Castells, L., Pubill, D., Camarasa, J., Valverde, O., & Escubedo, E. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13771 · Cited by 25 · see citing works
“Adolescence is a period of particular vulnerability to drug addiction (Cass et al., 2013), being a period of life in which different psychiatric disorders emerge (Paus et al.”
Background
MicroRNA Expression Profiling in the Prefrontal Cortex: Putative Mechanisms for the Cognitive Effects of Adolescent High Fat Feeding
Labouesse, M. A., Polesel, M., Clementi, E., Müller, F., Markkanen, E., Mouttet, F., Cattaneo, A., & Richetto, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-26631-x · Cited by 23 · see citing works
Maturation of Corticolimbic Functional Connectivity During Sensitive Periods of Brain Development
Yang, S., & Tseng, K. Y. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_239 · Cited by 23 · see citing works
Self-citation
Age- and sex-dependent effects of methamphetamine on cognitive flexibility and 5-HT2C receptor localization in the orbitofrontal cortex of Sprague-Dawley rats
Hankosky, E. R., Westbrook, S. R., Haake, R. M., Willing, J., Raetzman, L. T., Juraska, J. M., & Gulley, J. M. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.04.047 · Cited by 23 · see citing works
D1 receptor-mediated inhibition of medial prefrontal cortex neurons is disrupted in adult rats exposed to amphetamine in adolescence
Kang, S., Paul, K., Hankosky, E. R., Cox, C. L., & Gulley, J. M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.064 · Cited by 22 · see citing works
“Previous work in adolescent rats exposed to cocaine (Cass et al., 2013) or cannabinoids (Cass et al., 2014) has also demonstrated lasting changes (up to 35 days) in inhibitory tone in the mPFC.”
Background
Prefrontal α7nAChR Signaling Differentially Modulates Afferent Drive and Trace Fear Conditioning Behavior in Adolescent and Adult Rats
Fernández, A. M. M. M., Molla, H. M., Thomases, D. R., & Tseng, K. Y. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1941-20.2020 · Cited by 20 · see citing works
Self-citation
Cannabinoid CB1 receptor-sensitive neurodevelopmental processes and trajectories
Tseng, K. Y., & Molla, H. M. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03057-2 · Cited by 19 · see citing works
Self-citation
Adolescent‐onset GABA Aα1 silencing regulates reward‐related decision making
Butkovich, L. M., DePoy, L. M., Allen, A. G., Shapiro, L. P., Swanson, A. M., & Gourley, S. L. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12995 · Cited by 19 · see citing works
“As another example, cocaine exposure results in a hypo-metabolic state in the prefrontal cortex of mature rats, whereas the same cocaine exposure protocol applied in adolescence has the opposite effects (Cass et al., 2013).”
Background
Adolescent GBR12909 exposure induces oxidative stress, disrupts parvalbumin-positive interneurons, and leads to hyperactivity and impulsivity in adult mice
Khan, A., de Jong, L. A. W., Kamenski, M. E., Higa, K. K., Lucero, J. D., Young, J. W., Behrens, M. M., & Powell, S. B. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.11.022 · Cited by 18 · see citing works
“Adriani and Laviola (2002), Andersen et al. (2000), Beasley and Reynolds (1997), Benes and Berretta (2001), Berk et al. (2008), Cass et al. (2013), Ceylan et al. (2010), Gonchar et al. (2007), Hashimoto (2003), Kelley and Lang (1989), Lavoie et al. (2007), Leeson et al. (2009), Leo et al. (2009),…”
Repeated exposure to amphetamine during adolescence alters inhibitory tone in the medial prefrontal cortex following drug re-exposure in adulthood
Paul, K., Kang, S., Cox, C. L., & Gulley, J. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.04.018 · Cited by 18 · see citing works
High frequency stimulation-induced plasticity in the prelimbic cortex of rats emerges during adolescent development and is associated with an increase in dopamine receptor function
Kang, S., Cox, C. L., & Gulley, J. M. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.037 · Cited by 18 · see citing works
“Notably, peri-adolescent alterantions in dopamine signaling by cocaine exposure has been shown to abolish the HFS-induced LTD in the ventral hippocampus-mPFC circuit in adulthood (Cass et al., 2013).”
Influential
Enduring Effects of Adolescent Drug Exposure
Kuhn, C. M., Wilson, W., & Swartzwelder, S. H. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.030 · Cited by 13 · see citing works
“(3) study raises the concern that longlasting effects on the part of the brain that we rely on for our most sophisticated thinking may be changed permanently by this exposure.”
BackgroundInfluential
EGR-1 Expression in Catecholamine-synthesizing Neurons Reflects Auditory Learning and Correlates with Responses in Auditory Processing Areas
Dai, J., Chen, Y., & Sakata, J. T. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.03.032 · Cited by 13 · see citing works
Effects of amphetamine exposure during adolescence on behavior and prelimbic cortex neuron activity in adulthood
Sherrill, L. K., & Gulley, J. M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.05.028 · Cited by 12 · see citing works
“For example, D1and D2-mediated increases in GABAergic interneuron excitability occurs sometime between P36 and P50 in male rats (Tseng and O’Donnell, 2007).”
BackgroundInfluential
Adolescent oxycodone exposure inhibits withdrawal‐induced expression of genes associated with the dopamine transmission
Carpenter, M. D., Manners, M. T., Heller, E. A., & Blendy, J. A. (2020) · Addiction Biology · doi:10.1111/adb.12994 · Cited by 11 · see citing works
“netic modifications at genes associated with the dopamine transmission during adulthood at 1 and 28 days of withdrawal.(3,19) Adolescent mice were exposed to oxycodone from PND 28 to 56 to ensure the coverage of the entire period in which neurobehavioral discontinuities from younger and older mice are evident.”
Background
Prolonged withdrawal from cocaine self‐administration affects prefrontal cortex‐ and basolateral amygdala–nucleus accumbens core circuits but not accumbens GABAergic local interneurons
Purgianto, A., Weinfeld, M. E., & Wolf, M. E. (2016) · Addiction Biology · doi:10.1111/adb.12430 · Cited by 10 · see citing works
“This technique has proven effective in teasing out GABA components in other brain areas, and demonstrating changes in the GABA component after experimental manipulations (Thomases et al., 2013; Cass et al., 2013; Jayasinghe et al., 2015).”
BackgroundMethodInfluential
Age-dependent effects of (+)-MK801 treatment on glutamate release and metabolism in the rat medial prefrontal cortex
Zou, Y., Zhang, H., Chen, X., Ji, W., Mao, L., & Lei, H. C. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104503 · Cited by 10 · see citing works
Late-adolescent onset of prefrontal endocannabinoid control of hippocampal and amygdalar inputs and its impact on trace-fear conditioning behavior
Molla, H. M., Fernández, A. M. M. M., & Tseng, K. Y. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01844-z · Cited by 9 · see citing works
Self-citation
Age-dependent effects of vaping on the prefrontal cortex, ventral tegmental area, and nucleus accumbens
Henderson, B. J., Young, L. E., Olszewski, N. A., Tetteh-Quarshie, S., Maddox, S. K., Simpkins, M. A., Dudich, M. C., McGlauglin, M. S., Weinsweig, Z. C., & Cooper, S. Y. (2024) · Communications Biology · doi:10.1038/s42003-024-07272-5 · Cited by 8 · see citing works
“Previousstudieshaveshownthatotherdrugsof dependence(amphetamineandcocaine)givenatadolescenttimepoints produceanenhancementinmPFCneuronalexcitabilitybyattenuating GABAergicinhibitorysignalingandthispersistsintoadulthood 29,30 .”
mPFC DUSP1 mediates adolescent cocaine exposure‐induced higher sensitivity to drug in adulthood
Wei, X., Chang, J., Cheng, Z., Chen, W., Guo, H., Liu, Z., Mai, Y., Hu, T., Zhang, Y., Cai, Q., et al. (2023) · EMBO Reports · doi:10.15252/embr.202356981 · Cited by 9 · see citing works
“Cass et al (2013) found that adolescent cocaine administration produced mPFC disinhibition that endured throughout adulthood.”
GABA system in the prefrontal cortex involved in psychostimulant addiction
Shi, W., Li, M., Zhang, T., Yang, C., Zhao, D., & Bai, J. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae319 · Cited by 7 · see citing works
GABAergic polygenic risk for cocaine use disorder is negatively correlated with precuneus activity during cognitive control in African American individuals
Yang, B., Balodis, I. M., Hedy Kober, A., Worhunsky, P. D., Lacadie, C., Gelernter, J. E., & Potenza, M. N. (2020) · Addictive Behaviors · doi:10.1016/j.addbeh.2020.106695 · Cited by 7 · see citing works
Timing of Methamphetamine Exposure during Adolescence Differentially Influences Parvalbumin and Perineuronal Net Immunoreactivity in the Medial Prefrontal Cortex of Female, but Not Male, Rats
Brinks, A. S., Carrica, L. K., Tagler, D. J., Gulley, J. M., & Juraska, J. M. (2024) · Developmental Neuroscience · doi:10.1159/000538608 · Cited by 6 · see citing works
Exploring Cortical Interneurons in Substance Use Disorder: From Mechanisms to Therapeutic Perspectives
Shi, S., Chen, T., Su, H., & Zhao, M. (2025) · The Neuroscientist · doi:10.1177/10738584241310156 · Cited by 4 · see citing works
Very Long-Term Effects of Chronic Cocaine on Anxiety and Stress
Alves, C. J., Magalhães, A., Monteiro, P. R. R., & Summavielle, T. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-803750-8.00035-x · Cited by 4 · see citing works
IGF2 modulates behavioral and hippocampal changes induced by chronic cocaine exposure during adolescence in mice
Gil‐Rodríguez, S., Berdugo-Gómez, M., Claros, S., Romero‐Zerbo, S., Mañas‐Padilla, M. C., Gómez-Roldán, M. D. C., Blanco, E., Garcia‐Fernandez, M. I., & Santín, L. J. (2025) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2025.174095 · Cited by 2 · see citing works
Myocardial infarction sensitizes medial prefrontal cortex to inhibitory effect of locus coeruleus stimulation in rats
Glasgow, J., Koshman, Y. E., Samarel, A. M., Tseng, K. Y., & Scrogin, K. E. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4305-y · Cited by 2 · see citing works
“In both models, impaired cortical GABAergic function accompanies cognitive deficits (Cass et al. 2013; Tse et al. 2015).”
BackgroundSelf-citation
Single Cocaine Exposure Inhibits GABA Uptake via Dopamine D1-Like Receptors in Adolescent Mice Frontal Cortex
Kubrusly, R. C. C., Martins, R. S., Souza, L. D. S., de Carvalho, M. P., Borges-Martins, V. P. P., Sathler, M. F., Ferreira, D. D. P., Pereira, M. D. S., Pecinalli, N. R., Pandolfo, P., et al. (2020) · Neurotoxicity Research · doi:10.1007/s12640-020-00259-0 · Cited by 2 · see citing works
The DUSP1 on CaMKII-positive neurons in mPFC mediates adolescent cocaine exposure-induced higher sensitivity to cocaine during adulthoodPreprint
Wei, X., Chang, J., Cheng, Z., Chen, W., Guo, H., Liu, Z., Mai, Y., Hu, T., Zhang, Y., Cai, Q., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.26.505502 · Cited by 1 · see citing works
“al (26) found that adolescent cocaine administration produced mPFC 280 disinhibition that endured throughout adulthood.”
Background
Effects of Cocaine Sensitization on Drug Self-Administration, Mesocorticolimbic SAPAP Levels, and Prefrontal Ionotropic Glutamate Receptors
Summers, K. C. (2015) · doi:10.21007/etd.cghs.2015.0306
“55 blockade, which was later verified to occur in response to repeated cocaine exposure [192].”
Background
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Veldran, L. E. (2017)
Age-dependent effects of chronic amphetamine on prelimbic-nucleus accumbens circuit function and goal-directed behavior
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Long-term consequences of adolescent methylphenidate exposure on sustained attention and prelimbic PV+ interneuron maturation in rats
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Gil‐Rodríguez, S., Claros, S., Romero‐Zerbo, S., Zamorano-González, P., Berdugo-Gómez, M., Gómez-Roldán, M. D. C., Mañas‐Padilla, M. C., Martín‐Montañez, E., Garcia‐Fernandez, M. I., & Santín, L. J. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.7650008

Adolescent cocaine exposure enhances the GABAergic transmission in the prelimbic cortex of adult mice
Shi, P., Nie, J., Liu, H., Li, Y., Lu, X., Shen, X., Ge, F., Yuan, T., & Guan, X. (2019) · The FASEB Journal · doi:10.1096/fj.201802192rr · Cited by 28 · see citing works
CB1 cannabinoid receptor stimulation during adolescence impairs the maturation of GABA function in the adult rat prefrontal cortex
Cass, D. K., Flores-Barrera, E., Thomases, D. R., Vital, W. F., Caballero, A. C., & Tseng, K. Y. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.14 · Cited by 181 · see citing works
Self-citation
mGlu 1 Activation Reverses Persistent Deficits in Prefrontal Cortex Inhibitory Transmission and Working Memory Induced by Adolescent Cocaine Exposure
Luessen, D. J., Gallinger, I. M., & Conn, P. J. (2022) · The FASEB Journal · doi:10.1096/fasebj.2022.36.s1.r2232
Metabotropic mGlu1 Receptor Regulation of Cortical Inhibition and Cognitive Function: Implications in Adolescent Cocaine Exposure
Luessen, D. J., Gallinger, I. M., Wolfe, B., & Conn, P. J. (2023) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.122.138580
Altered Attention and Prefrontal Cortex Gene Expression in Rats after Binge-Like Exposure to Cocaine during Adolescence
Black, Y. D., Maclaren, F. R., Naydenov, A. V., Carlezon, W. A., Baxter, M. G., & Konradi, C. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2391-06.2006 · Cited by 91 · see citing works

Authors: Cass, D. K., Thomases, D. R., Caballero, A., & Tseng, K. Y.
Affiliations: Rosalind Franklin University of Medicine and Science (US)
Corresponding author: Tseng, Kuei Y.
ORCID: Caballero, Adriana
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2013-10
Volume: 74
Issue: 7
Pages: 490-501
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2013.02.021
PMC: PMC3722277
OpenAlex: W2084965555
Cited by: 63
References: 76
Citations by year: 2026: 3 · 2025: 4 · 2024: 4 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 7 · 2019: 2 · 2018: 8 · 2017: 4 · 2016: 15 · 2015: 2 · 2014: 5 · 2013: 4
FWCI: 4.25
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (DA004093, MH086507)
Rosalind Franklin University of Medicine and Science
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: cocaine, adolescent drug exposure, medial prefrontal cortex, GABAergic inhibition, parvalbumin, disinhibition, ventral hippocampus, beta and gamma oscillations, local field potentials, developmental disruption, addiction liability, substance abuse risk
MeSH terms: Age Factors, Animals, Benzodiazepines, Cocaine, Hippocampus, Male, Neural Inhibition, Neural Pathways, Picrotoxin, Receptors, GABA-A, Thiophenes, Rats, Sprague-Dawley, Prefrontal Cortex, GABA Antagonists, GABA Modulators, Rats, GABAergic Neurons

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Developmental disruption of gamma-aminobutyric acid function in the medial prefrontal cortex by noncontingent cocaine exposure during early adolescence

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