Physiological and morphological properties of accumbens core and shell neurons recorded in vitro

The morphology and electrophysiological properties of neurons in the nucleus accumbens were studied using intracellular recording techniques in rat brain slices maintained in vitro. Neurons were subdivided according to their location in the shell or core region of the nucleus accumbens. Most of the cells in both regions had small to medium‐sized (15.8 ± 2.8 μM) somata with densely spinous dendrites, somewhat similar to the striatal medium spiny neuron. However, minor morphological differences between neurons from accumbens core and shell regions were found, such as fewer primary dendrites in shell neurons than in the core (3.8 ± 0.8 vs. 4.4 ± 1.0) and the spatial organization of their dendritic trees. In general, the passive membrane properties of neurons in each region were similar. However, shell neurons appeared to be less excitable in nature, as suggested by (1) a faster time constant, (2) the absence of TTX‐insensitive events resembling low‐threshold spikes, and (3) the lower probability of evoking spikes in shell neurons by stimulation of amygdaloid or cortical afferents in comparison to the responses of coreneurons to cortical afferent stimulation. In most nucleus accumbens neurons the action potentials evoked by membrane depolarization were preceded by a slow Ca2+‐dependent depolarization and showed firing‐frequency adaptation. Following TTX administration, all‐or‐none spike‐like events resembling high‐threshold calcium spikes were observed in both regions. In summary, except for minor differences, most of the properties of core and shell neurons are similar, supporting their characterization as subdivisions of a single structure. Therefore, differences in the functional properties of these neuronal populations are likely to be due to their distinct connectivity patterns. © 1993 Wiley‐Liss, Inc.

[1]  S. Snyder,et al.  Amphetamine psychosis: a "model" schizophrenia mediated by catecholamines. , 1973, The American journal of psychiatry.

[2]  R. Llinás,et al.  Morphological artifacts induced in intracellularly stained neurons by dehydration: Circumvention using rapid dimethyl sulfoxide clearing , 1985, Neuroscience.

[3]  T. Kita,et al.  Effects of 4-aminopyridine (4-AP) on rat neostriatal neurons in an in vitro slice preparation , 1985, Brain Research.

[4]  W. Cowan,et al.  A note on the connections and development of the nucleus accumbens , 1975, Brain Research.

[5]  A. Dray The striatum and substantia nigra: A commentary on their relationships , 1979, Neuroscience.

[6]  Bruno Giros,et al.  Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics , 1990, Nature.

[7]  J. Price,et al.  Sources of presumptive glutamergic/aspartergic afferents to the rat ventral striatopallidal region , 1987, The Journal of comparative neurology.

[8]  G. Mogenson,et al.  Nucleus accumbens to globus pallidus GABA projection: Electrophysiological and iontophoretic investigations , 1980, Brain Research.

[9]  P. Calabresi,et al.  Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: Evidence for D1 receptor involvement , 1987, Neuroscience.

[10]  H. Groenewegen,et al.  Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid , 1980, Neuroscience.

[11]  R. Romo,et al.  In vivo presynaptic control of dopamine release in the cat caudate nucleus—III. Further evidence for the implication of corticostriatal glutamatergic neurons , 1986, Neuroscience.

[12]  T. Pasik,et al.  A Golgi study of neuronal types in the neostriatum of monkeys , 1976, Brain Research.

[13]  G. P. Smith,et al.  Efferent connections and nigral afferents of the nucleus accumbens septi in the rat , 1978, Neuroscience.

[14]  Intracellular Electrophysiological Techniques , 1990 .

[15]  A. Grace,et al.  Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  P. Stanzione,et al.  Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. , 1988, The Journal of physiology.

[17]  A. Grace Regulation of spontaneous activity and oscillatory spike firing in rat midbrain dopamine neurons recorded in vitro , 1991, Synapse.

[18]  C. W. Ragsdale,et al.  Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat , 1988, The Journal of comparative neurology.

[19]  C. Y. Yim,et al.  Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine , 1982, Brain Research.

[20]  W. Rall Time constants and electrotonic length of membrane cylinders and neurons. , 1969, Biophysical journal.

[21]  R. North,et al.  Inward rectification in rat nucleus accumbens neurons. , 1989, Journal of neurophysiology.

[22]  R. Llinás,et al.  Electrophysiology of mammalian thalamic neurones in vitro , 1982, Nature.

[23]  L. Heimer,et al.  New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata , 1988, Neuroscience.

[24]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—1. Identification and characterization , 1983, Neuroscience.

[25]  G. Mogenson,et al.  An electrophysiological study of the neural projections from the hippocampus to the ventral pallidum and the subpallidal areas by way of the nucleus accumbens , 1985, Neuroscience.

[26]  Akinori Akaike,et al.  Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate nucleus neurons in vitro , 1987, Brain Research.

[27]  L. Swanson,et al.  Neural projections from nucleus accumbens to globus pallidus, substantia innominata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Cassell,et al.  Morphology of peptide‐immunoreactive neurons in the rat central nucleus of the amygdala , 1989, The Journal of comparative neurology.

[29]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[30]  Bruno Giros,et al.  Localization of dopamine D3 receptor mRNA in the rat brain using in situ hybridization histochemistry: comparison with dopamine D2 receptor mRNA , 1991, Brain Research.

[31]  S. Pr,et al.  Differential effects of microinjections of d-amphetamine into the nucleus accumbens or the caudate putamen on the rat's ability to ignore an irrelevant stimulus. , 1982 .

[32]  D. Sanchez,et al.  Properties and ionic basis of the action potentials in the periaqueductal grey neurones of the guinea‐pig. , 1991, The Journal of physiology.

[33]  R. M. Beckstead An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat , 1979, The Journal of comparative neurology.

[34]  J. E. Vaughn,et al.  The GABA Neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry , 1979, The Journal of comparative neurology.

[35]  M. Sugimori,et al.  Response properties and electrical constants of caudate nucleus neurons in the cat. , 1978, Journal of neurophysiology.

[36]  R. Wise,et al.  Effects of nucleus accumbens amphetamine on lateral hypothalamic brain stimulation reward , 1988, Brain Research.

[37]  H. Higashi,et al.  Hyperpolarizing and depolarizing actions of dopamine via D-1 and D-2 receptors on nucleus accumbens neurons , 1986, Brain Research.

[38]  C. Gerfen The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems , 1984, Nature.

[39]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[40]  J. W. Lighthall,et al.  A short duration GABAergic inhibition in identified neostriatal medium spiny neurons: In vitro slice study , 1983, Brain Research Bulletin.

[41]  F. J. White,et al.  Differential effects of classical and atypical antipsychotic drugs on A9 and A10 dopamine neurons. , 1983, Science.

[42]  P. Schwindt,et al.  Properties of subthreshold response and action potential recorded in layer V neurons from cat sensorimotor cortex in vitro. , 1984, Journal of neurophysiology.

[43]  M. Olds Enhanced dopamine receptor activation in accumbens and frontal cortex has opposite effects on medial forebrain bundle self-stimulation , 1990, Neuroscience.

[44]  T. W. Berger,et al.  Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—II. In vitro analysis , 1992, Neuroscience.

[45]  D. Pfaff,et al.  Autoradiographic tracing of nucleus accumbens efferents in the rat , 1976, Brain Research.

[46]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[47]  M. Sugimori,et al.  Ionic currents and firing patterns of mammalian vagal motoneurons In vitro , 1985, Neuroscience.

[48]  C. Pennartz,et al.  Differential membrane properties and dopamine effects in the shell and core of the rat nucleus accumbens studied in vitro , 1992, Neuroscience Letters.

[49]  N. Swerdlow,et al.  Dopamine, schizophrenia, mania, and depression: Toward a unified hypothesis of cortico-striatopallido-thalamic function , 1987, Behavioral and Brain Sciences.

[50]  H. Kita,et al.  Amygdaloid projections to the frontal cortex and the striatum in the rat , 1990, The Journal of comparative neurology.

[51]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

[52]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[53]  J. Hubbard,et al.  Characterization of fimbria input to nucleus accumbens. , 1985, Journal of neurophysiology.

[54]  L. Heimer,et al.  Ventral striatopallidal parts of the basal ganglia in the rat: I. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity , 1988, The Journal of comparative neurology.

[55]  G Bernardi,et al.  Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis. , 1990, Journal of neurophysiology.

[56]  J. Walsh,et al.  Neurophysiological maturation of cat caudate neurons: Evidence from in vitro studies , 1991, Synapse.

[57]  H. T. Chang,et al.  Vasoactive intestinal polypeptide (VIP) immunoreactive elements in the caudal ventral striatum of the rat: A light and electron microscopic study , 1991, Brain Research Bulletin.

[58]  D. A. Brown,et al.  Persistent slow inward calcium current in voltage‐clamped hippocampal neurones of the guinea‐pig. , 1983, The Journal of physiology.

[59]  H. Groenewegen,et al.  The distribution and compartmental organization of the cholinergic neurons in nucleus accumbens of the rat , 1989, Neuroscience.

[60]  P. Calabresi,et al.  Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity , 1987, Neuroscience.

[61]  L. Heimer,et al.  Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study , 1985, Neuroscience.

[62]  A. McDonald,et al.  Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain , 1991, Neuroscience.

[63]  T. Kita,et al.  Passive electrical membrane properties of rat neostriatal neurons in an in vitro slice preparation , 1984, Brain Research.

[64]  G. Mogenson,et al.  Electrophysiological responses of neurones in the nucleus accumbens to hippocampal stimulation and the attenuation of the excitatory responses by the mesolimbic dopaminergic system , 1984, Brain Research.

[65]  A. Grace,et al.  In Vivo and in Vitro Intracellular Recordings from Rat Midbrain Dopamine Neurons a , 1988, Annals of the New York Academy of Sciences.

[66]  H. Higashi,et al.  Membrane properties and synaptic responses of the guinea pig nucleus accumbens neurons in vitro. , 1989, Journal of neurophysiology.

[67]  G Bernardi,et al.  Involvement of GABA systems in feedback regulation of glutamate‐and GABA‐mediated synaptic potentials in rat neostriatum. , 1991, The Journal of physiology.

[68]  D. S. Zahm,et al.  Specificity in the projection patterns of accumbal core and shell in the rat , 1991, Neuroscience.

[69]  J. Féger,et al.  Identification of different subpopulations of neostriatal neurones projecting to globus pallidus or substantia nigra in the monkey: A retrograde fluorescence double-labelling study , 1984, Neuroscience Letters.

[70]  R Llinás,et al.  Electrophysiology of mammalian tectal neurons in vitro. I. Transient ionic conductances. , 1988, Journal of neurophysiology.

[71]  P. Schwindt,et al.  Effects of barium on cat spinal motoneurons studied by voltage clamp. , 1980, Journal of neurophysiology.

[72]  W. B. Orr,et al.  Evidence for two functionally distinct subpopulations of neurons within the rat striatum , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  S. T. Kitai,et al.  Morphological and physiological properties of neostriatal neurons: An intracellular horseradish peroxidase study in the rat , 1982, Neuroscience.

[74]  E. W. Powell,et al.  Connections of the nucleus accumbens , 1976, Brain Research.

[75]  P. Schwindt,et al.  Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. , 1988, Journal of neurophysiology.

[76]  A. Cools,et al.  Evidence that dopamine in the nucleus accumbens is involved in the ability of rats to switch to cue-directed behaviours , 1991, Behavioural Brain Research.

[77]  D. Kernell,et al.  Limits of usefulness of electrophysiological methods for estimating dendritic length in neurones , 1982, Journal of Neuroscience Methods.

[78]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—2. Action potential generating mechanisms and morphological correlates , 1983, Neuroscience.

[79]  T. Robbins,et al.  The basolateral amygdala-ventral striatal system and conditioned place preference: Further evidence of limbic-striatal interactions underlying reward-related processes , 1991, Neuroscience.

[80]  M. Martres,et al.  The third dopamine receptor (D3) as a novel target for antipsychotics. , 1992, Biochemical pharmacology.

[81]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[82]  A. Grace Evidence for the functional compartmentalization of spike generating regions of rat mdbrain dopamine neurons recorded in vitro , 1990, Brain Research.

[83]  B. Bunney,et al.  Typical and atypical neuroleptics: differential effects of chronic administration on the activity of A9 and A10 midbrain dopaminergic neurons , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  H. T. Chang,et al.  Intracellular recordings from rat nucleus accumbens neurons in vitro , 1986, Brain Research.

[85]  T. Kita,et al.  Local stimulation induced GABAergic response in rat striatal slice preparations: Intracellular recordings on QX-314 injected neurons , 1985, Brain Research.

[86]  E. Cherubini,et al.  An inward calcium current underlying regenerative calcium potentials in rat striatal neurons in vitro enhanced by BAY K 8644 , 1987, Neuroscience.

[87]  S. Sesack,et al.  In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other , 1990, Brain Research.

[88]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[89]  S T Kitai,et al.  Version unknown SOURCE ( OR PART OF THE FOLLOWING SOURCE ) : Type article Title Hippocampal inputs to identified neurons in an in vitro slice preparation of the rat nucleus accumbens : evidence for feed-forward inhibition , 2003 .

[90]  J. Scheel-Krüger,et al.  Cueing effects of amphetamine and LSD: elicitation by direct microinjection of the drugs into the nucleus accumbens. , 1986, European journal of pharmacology.