Metabolic Mapping of the Brain During Rewarding Self-Stimulation

Porrino, Linda J.; Esposito, Ralph; Seeger, Thomas; Crane, Alison M.; Pert, Agu; Sokoloff, Louis

doi:10.1126/science.6710145

Cited by 111 publications

(40 citation statements)

References 8 publications

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“…These results indicate that the overall pattern of cerebral metabolic activity associated with the behavioral pattern of self-stimulation to the VTA involves the activation of a discretely organized neural system with representation at all levels of the neuraxis. Furthermore, recent work by Porrino et al (25) indicates that this pattern of neural activity in self-stimulating animals is distinctly different from that seen when nonresponse contingent stimulation is delivered by the experimenter (at rates and current parameters comparable to those used in the present study) to VTA placements that had previously been shown to support self-stimulation at these same parameters.…”

Section: Discussioncontrasting

confidence: 71%

Changes in local cerebral glucose utilization during rewarding brain stimulation.

Esposito¹,

Porrino²,

Seeger³

et al. 1984

Proc. Natl. Acad. Sci. U.S.A.

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The quantitative 2-deoxy[14C]glucose method was used to determine local cerebral glucose utilization in unrestrained rats responding (lever-press) for rewarding electrical stimulation to area A10 (ventral tegmental area) and in similarly implanted inactive controls. Self-stimulation was associated with significant increases in metabolic activity, highly circumscribed in the ventral tegmental area, that continued rostrally within a rather compact zone of activity through the medial forebrain bundle, extending via the diagonal band of Broca to the level of the preoptic area. In the forebrain terminal areas bilateral increases in local cerebral glucose utilization were noted in the nucleus accumbens, lateral septum, hippocampus, and the mediodorsal nucleus of the thalamus. Ipsilateral (i.e., side of stimulation) increases in glucose utilization were noted in the bed nucleus of the stria terminalis, the basolateral and central amygdaloid nuclei, and the medial prefrontal cortex. Caudal to the stimulation site, increases in glucose utilization were found in the midline dorsal raphe, the ipsilateral pontine gray, medial parabrachial nucleus, and the locus coeruleus. Significant bilateral increases were noted in various sensory and motor areas. These results indicate that rather than a diffuse pattern of activity, rewarding brain stimulation is associated with discrete activation of specific neuronal projection fibers and selective terminal sites.The discovery that rats will work to receive brief trains of electrical stimulation to discrete areas of their brains (1) was soon followed by similar demonstrations in diverse species from goldfish to higher primates, including man (2). This phenomenon has generally been interpreted as reflecting a very fundamental neurophysiological mechanism(s) of widespread and adaptive evolutionary significance (3)(4)(5). Early attempts to delineate the critical neural circuitry that mediates the reinforcing or rewarding aspects of this behavior yielded little specific information (6,7). Subsequent studies, however, suggested an important relationship between certain ascending catecholaminergic pathways and this behavior (8, 9). In particular, cogent evidence has been adduced for a critical, albeit nonexclusive, role for ascending dopaminergic fibers in the mediation of self-stimulation derived from cell bodies in the ventral tegmental area (VTA) (9), corresponding to area A10 of Dahlstrom and Fuxe (10). Because of the ability of the 2-deoxy[14C]glucose autoradiographic method to assess local metabolic and functional neural activities simultaneously throughout the entire brain (11), it was used in this study to examine the overall pattern of sensory, motor, and integrative neural activity during rewarding selfstimulation to the VTA. MATERIALS AND METHODSMale albino Sprague-Dawley rats (-350 g) were anesthetized with chloral hydrate and stereotaxically implanted unilaterally with bipolar platinum electrodes (0.125 mm diameter) aimed at the VTA (coordinates: A + 3.4, L ± 1.0, V + 2....

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Section: Discussioncontrasting

confidence: 71%

Changes in local cerebral glucose utilization during rewarding brain stimulation.

Esposito¹,

Porrino²,

Seeger³

et al. 1984

Proc. Natl. Acad. Sci. U.S.A.

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“…Application of this strategy is already obvious in studies which have successfully identified the brain regions that get activated following SS of MFB sites. In these studies the 2-deoxyglucose autoradiography, 13,16,34,35 or the cytochrome oxidase staining 3 were used. In both techniques the neuronal activation is quantitatively determined through optical density measurements.…”

mentioning

confidence: 99%

Ventral pallidum self-stimulation induces stimulus dependent increase in c-fos expression in reward-related brain regions

et al. 1997

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“…The pattern of regional metabolic activation of the rat brain after rewarding electrical self-stimulation of the VTA or cocaine is quite different from the pattern seen after stimulation of the same area by the experimenter (Howell, Votaw, Goodman, & Lindsey, 2010;Porrino et al, 1984). It is widely recognized that hospitalized patients to whom high doses of opioid drugs are administered by treatment personnel for relief of severe pain frequently develop tolerance and physical dependence, yet they seldom become compulsive drug seekers and users (O'Brien, 2001).…”

Section: Evidence That Does Not Support An Exclusively Neurobiologicamentioning

confidence: 85%

Neurobiological research on addiction: What value has it added to the concept?

Kalant

2015

IJADR

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The initial goal of neurobiological research on addiction was to identify the neural mechanisms involved in the mediation and expression of addictive behavior. More recently, however, it has attributed causal roles to these mechanisms, as illustrated by the definition of addiction as a brain disease caused by chronic exposure to a drug. This concept carries a number of implications that can be assessed experimentally and clinically. None of these implications is borne out by the currently available evidence. The interactions of neuronal systems involved in addiction are also involved in adaptation to experience and environmental change. Much of the neurobiological research to date has not differentiated between causes of addiction, neuronal mechanisms that are activated by them, and risk factors that contribute to individual vulnerability. It has largely ignored the important experiential and environmental influences known to affect the prevalence of addiction in different populations or different times, and it has so far directed much less attention to other forms of addiction-like behavior that do not involve drugs. These failures are not inherent in neurobiological research but require reorientation of objectives, including more emphasis on the study of mechanisms by which environment and experience, including drug experience, can determine whether genetic risk factors are expressed or remain dormant and can direct neuroadaptive mechanisms toward alternative outcomes.

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Metabolic Mapping of the Brain During Rewarding Self-Stimulation

Cited by 111 publications

References 8 publications

Changes in local cerebral glucose utilization during rewarding brain stimulation.

Changes in local cerebral glucose utilization during rewarding brain stimulation.

Ventral pallidum self-stimulation induces stimulus dependent increase in c-fos expression in reward-related brain regions

Neurobiological research on addiction: What value has it added to the concept?

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