Behavioral methods for inferring anatomical linkage between rewarding brain stimulation sites.

Shizgal, Peter; Bielajew, Catherine; Corbett, Dale; Skelton, Ronald W.; Yeomans, John S.

doi:10.1037/h0077668

Cited by 191 publications

(122 citation statements)

References 25 publications

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“…Not all of the results of the unilateral two-electrode experiment resemble those in Figure 7, Panel A. In fact, some curves look like those obtained from subjects with bilateral Shizgal et al, 1980, andYeomans, 1979. ) electrodes.…”

Section: Two-electrode Experimentsmentioning

confidence: 48%

“…During the past decade, various long-axon, catecholaminergic components of the MFB have been suggested to serve this role. Shizgal et al (1980) reasoned that if such longaxon neurons were in fact the directly stimulated substrate for MFB self-stimulation, then it should be possible to demonstrate collision effects when two ipsilateral MFB self-stimulation sites were stimulated concurrently.…”

Section: Two-electrode Experimentsmentioning

confidence: 99%

“…Since no direct axonal connections have been demonstrated between the two contralateral hypothalamic nuclei, Shizgal et al (1980) chose bilateral, lateral hypothalamic stimulation as a test case. The results of this two-electrode paired-pulse experiment are shown in Figure 7, Panel B.…”

Section: Two-electrode Experimentsmentioning

confidence: 99%

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A portrait of the substrate for self-stimulation.

Gallistel

Shizgal²,

Yeomans³

1981

Psychological Review

353

186

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Quantitative properties of the neural system mediating the rewarding and priming effects of medial forebrain bundle (MFB) stimulation in the rat have been determined by experiments that trade one parameter of the electrical stimulus against another. The first-order neurons in this substrate are for the most part long, thin, myelinated axons, coursing in the MFB and ventral tegmentum, with absolute refractory periods in the range .5-1.2 msec and conduction velocities of 2-8 m/sec. Local potentials in these axons decay with a time constant of about .1 msec. A supernormal period follows the recovery from refractoriness. These axons integrate current over exceptionally long intervals, accommodate slowly, and fire on the break of prolonged anodal pulses. These properties rule out the hypothesis that catecholamine pathways constitute the first-order axons. The second-order (postsynaptic) part of the substrate shows surprisingly simple spatial and temporal integrating characteristics. We examine the logic that permits conclusions of this sort to be derived from behavioral data and the role of these derivations in establishing neurobehavioral linkage hypotheses.In this article we describe properties of the neural tissue whose excitation eventuates in the reinforcing and motivating effects of electrical stimulation of the medial forebrain bundle (MFB) in the rat. The goal of the research is to identify these systems by anatomical and electrophysiological methods, thus providing physiological psychology with a model for studying the neurophysiological bases of learning and motivation in a higher vertebrate.The properties of the substrate for selfstimulation described in this article have been inferred from behavioral trade-off experiments-experiments that determine the value of one parameter of stimulation (e.g., current intensity) required to produce a criterion level of performance at each setting of another parameter (e.g., pulse duration). We review experiments of this kind in selfstimulation while examining two theoretical questions: (a) Why do behavioral trade-off functions have the power to reveal quantitative properties of the substrate for the behavior? and (b) Why must trade-off experiments play a pivotal role in relating anatomical and electrophysiological data to the behavioral phenomenon?Using microelectrodes, physiological psychologists have long been able to examine the response of single neurons to a behaviorally significant stimulus, such as rewarding brain stimulation (Rolls, 1975). The advent of 2-deoxyglucose autoradiography makes it possible to visualize a whole range of neural systems activated by such a stimulus (Figure 1). The existence of powerful techniques for directly revealing nervous activity confronts us with a conceptual problem that physiological psychology shares with other reductionist disciplines: How may one establish that a system defined by observations at one level of analysis explains phe-228

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Section: Two-electrode Experimentsmentioning

confidence: 48%

Section: Two-electrode Experimentsmentioning

confidence: 99%

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A portrait of the substrate for self-stimulation.

Gallistel

Shizgal²,

Yeomans³

1981

Psychological Review

353

186

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show abstract

“…U sing the pulse-pair technique (Shizgal, Bielajew, Corbett, Skelton, & Yeomans, 1980), the manner in which the neurons mediating the aversive consequences of stimulation link these two sites is currently being investigated in our laboratory. Such data may choose between the possibilities outlined above.…”

Section: Morphine and Brain Stimulation 377 General Discussionmentioning

confidence: 99%

A comparison between the effects of morphine on the rewarding and aversive properties of lateral hypothalamic and central gray stimulation

et al. 1980

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“…Thus, the search for the neural processes underlying positive reinforcement has most often focused on pathways traveling through the medial forebrain bundle. Studies of electrical brain self-stimulation have identified the medial forebrain bundle as a prime substrate for reward (Olds and Olds, 1965;Rolls, 1975;Wise and Bozarth, 1984), and the neurons directly stimulated by the electrode are apparently myelinated, fast-conducting, and descending neurons that have short refractory periods (Shizgal et al, 1980;Yeomans, 1989).…”

mentioning

confidence: 99%

The tegmental pedunculopontine nucleus: a brain-stem output of the limbic system critical for the conditioned place preferences produced by morphine and amphetamine

1989

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The potent reinforcing properties of psychoactive drugs have been attributed to the activation of motivational processes localized to the limbic system. We investigated the role of 2 specific outputs of the forebrain limbic system, the tegmental pedunculopontine nucleus (TPP) and the periacqueductal gray (PAG) of the pons-midbrain, in the positive motivational effects of morphine and amphetamine. We now report that the TPP, but not the PAG nor other nearby regions, is a critical site in the neural system subserving the rewarding effects of both opiates and stimulants. Bilateral ibotenic acid lesions of the TPP blocked the positive reinforcing effects of both morphine and amphetamine in naive rats as measured in a conditioned place preference paradigm. However, TPP lesioned animals were still capable of acquiring a conditioned place preference to an environment paired with the peripheral opiate antagonist methylnaltrexone. This suggested that TPP lesions did not cause nonspecific deficits in the basic learning mechanisms underlying conditioned place preferences. Furthermore, while the TPP was critical for the acquisition of a conditioned preference to an environment paired with morphine in naive rats, rats that had acquired a morphine conditioned place preference prior to the lesions were capable of retaining and demonstrating these place preferences after lesions of the TPP. This again demonstrates that TPP lesions are producing an unconditioned deficit in motivation rather than a deficit in learning or memory. Finally, direct comparisons of the place preference data of individual animals with their correspondent TPP lesion sites indicated that the most effective lesions overlapped to a greater degree TPP perikarya with descending, rather than ascending, axons. This suggests that motivational information generated by drug stimuli acting at “upstream” neural structures flows in a descending direction through the TPP region of the brain stem. These results suggest that opiates and stimulants must ultimately activate a single brain-stem substrate in order to have a positive motivational impact. It is hypothesized that the neural circuits mediating the rewarding effects of drug stimuli acting at forebrain sites exit the limbic system in the TPP region of the brain stem, where motivation may ultimately influence or be isomorphic with the elicitation of motor responses subserving approach and exploration.

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Behavioral methods for inferring anatomical linkage between rewarding brain stimulation sites.

Cited by 191 publications

References 25 publications

A portrait of the substrate for self-stimulation.

A portrait of the substrate for self-stimulation.

A comparison between the effects of morphine on the rewarding and aversive properties of lateral hypothalamic and central gray stimulation

The tegmental pedunculopontine nucleus: a brain-stem output of the limbic system critical for the conditioned place preferences produced by morphine and amphetamine

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