A portrait of the substrate for self-stimulation.

Abstract

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

Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: Implications for intracranial self-stimulation

“…Indeed, with a continuous ICS schedule, dopamine release is suppressed (28,36,37). Although direct activation of dopaminergic neurons is unnecessary for ICS (20), we purposely used stimulation parameters that orthodromically activate dopaminergic neurons (15). These parameters, used in conjunction with the FR1, TO10Љ schedule, support stable dopamine release during ICS and complement those of Yavich and Tiihonen (37), who showed that stable dopamine release can occur during ICS on an FR8 schedule.…”

“…The observed E-type responses (Fig. 6) may be the critical first-stage neurons for ICS (20). However, we did not pharmacologically investigate their GABAergic properties.…”

“…However, several other neuronal systems project through the MFB and are activated by its stimulation. For example, a descending, myelinated neuronal pathway has been identified as central to maintenance of ICS (20). A GABAergic pathway, comprising 36% of VTA projection neurons (21), ascends to the NAc (22) and can also be activated in anticipation of a reinforced response for ICS (23).…”

Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation

“…Although calculations and experiments indicate direct depolarization is less likely with stimuli delivered to the cell bodies (22)(23)(24), electrically evoked dopamine release could arise from transsynaptic activation of glutamatergic or cholinergic afferents in the VTA. Indeed, by using much different stimulation parameters and locations, it has been shown that ICSS can be supported by stimulations that activate descending, nondopaminergic fibers and secondarily effect dopamine neurotransmission (25)(26)(27).…”

Neural basis of utility estimation

“…As Shizgal and Conover have argued [13**], such stimulation is unlikely to simulate a naturalistic signal in a system, such as the auditory nerve, that employs a spatiotemporal code to represent multiple stimulus dimensions. Even more problematic for the notion that the directlystimulated stage of the system encodes multidimensional information is the finding that the utility of BSR can be held constant as the current and frequency of the stimulation are varied in a compensatory fashion [14,15]. A high-current, low-frequency train can be adjusted so that it is preferred equally to a low-current, high-frequency train.…”