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Accumbens dopamine and the regulation of effort in food-seeking behavior: modulation of work output by different ratio or force requirements

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Abstract

It has been suggested that depletions of accumbens dopamine (DA) make rats more sensitive to work-related response costs. One way of controlling work costs in operant tasks has been to use fixed-ratio (FR) schedules with different ratio requirements. In addition to using ratio requirements to control response costs, investigators also can employ different force requirements. In the present study, different groups of rats were trained on two schedules (FR 1 and FR 5) and weights were placed on the levers 2 days each week. In the FR 5 studies, two different weights were used (32 or 64 g), while three different weights were used in the FR 1 studies (32, 64, or 96 g). After baseline training, rats received intra-accumbens injections of either 6-OHDA to deplete DA, or ascorbate vehicle as the control. The effects of DA depletions were highly schedule-dependent. DA-depleted animals on the FR 5 schedule showed reductions in responding across the different weight conditions. In contrast, DA depletion did not significantly suppress FR 1 responding under any conditions. Addition of weights to the levers reduced responding on the FR 1 and FR 5 schedules, but did not enhance sensitivity to DA depletion. Thus, rats with accumbens DA depletions were sensitive to different ratio requirements, yet they were relatively insensitive to different force requirements within the range tested. These studies indicate that DA depletions make animals sensitive to temporal or rate components of work that greatly influence responding on ratio schedules.

Introduction

Considerable research indicates that the nucleus accumbens is a component of the brain circuitry that regulates instrumental behavior [4], [6], [20], [30], [31]. Instrumental behavior is a very complex and multi-faceted phenomenon, and there are several factors that influence response output. Primary motivational processes, Pavlovian and instrumental associative factors, and work requirements of the schedule, all serve as factors that regulate instrumental performance [1], [5], [8], [14], [16], [19], [21], [26], [27], [31], [33], [40]. Although there is substantial evidence indicating that dopamine (DA) in the nucleus accumbens does not mediate primary food motivation, reinforcement and appetite (for reviews see [30], [31], [33]), many studies point to a role for accumbens DA in the modulation of several important aspects of incentive motivation [3], [4], [6], [13], [22], [23], [26], [27], [30], [33]. One of the hypothesized functions of nucleus accumbens DA is involvement in the processes that enable organisms to overcome work-related response costs in instrumental responding [30], [31], [33], [36]. Several studies have shown that accumbens DA depletions alter response allocation in behavioral choice procedures that involve various reinforcement values and response costs [10], [11], [12], [31], [32], [33], [36], [39]. Moreover, considerable research has demonstrated that the effects of accumbens DA depletions on instrumental lever pressing are highly dependent upon the schedule being tested. Performance on schedules that have minimal response requirements is relatively unaffected by accumbens DA depletions, while other types of schedules are more severely disrupted [1], [2], [25], [28], [31], [33], [34], [39].

The present studies were designed to investigate how work-related factors interact with the effects of accumbens DA depletions. One way of varying work requirements on lever pressing schedules is to vary the ratio requirement (i.e. the number of lever presses required for each reinforcement). Previous work has shown that increased ratio requirements make animals more sensitive to the effects of accumbens DA depletions [1], [9], [37]. In addition to using ratio requirements to control response costs, investigators also can employ different force requirements. In the present study, different groups of rats were trained on two fixed-ratio (FR) schedules (FR 1 or FR 5) and weights were placed on the levers two alternating days each week. In the FR 5 studies, two different weights were used (32 or 64 g), while three different weights were used in the FR 1 studies (32, 64, or 96 g). After baseline training, rats received intra-accumbens injections of either 6-OHDA to deplete DA, or ascorbate vehicle as the control. Previous studies have shown that the FR 1 schedule is relatively insensitive to the effects of accumbens DA depletions [1], [25], [34]. In contrast, accumbens DA depletions have been shown to affect FR 5 performance [35], [39]. Thus, it was expected that the effects of accumbens DA depletions would be schedule-dependent. Predictions about the possible interaction between DA depletions and weight requirements were somewhat problematic, however. On the one hand, if accumbens DA depletions produce effects that make animals more sensitive to increased work requirements across a variety of conditions, then increasing the weight on the lever should make animals more sensitive to DA depletions. Nevertheless, it is not clear from the literature that dopaminergic manipulations interact with all types of work requirements in an equivalent manner. Previous research with several different paradigms has shown that the DA antagonist haloperidol, when administered in systemic doses that affected response rate and temporal characteristics of lever pressing, had no effects on peak response force [17], [18], [24], [41]. Thus, the present studies were designed to determine if the combined effects of weight on the lever and of DA depletion would be additive or synergistic under the two schedule conditions being studied.

Section snippets

Subjects

A total of 109 male Sprague–Dawley rats (Harlan Sprague–Dawley, Indianapolis, IN, USA) were used in these experiments. Animals were housed in a colony maintained at a constant temperature (23 °C) with a 12 h light/12 h dark cycle (lights on at 07:00 h). All rats weighed between 280 and 335 g at the beginning of the study. Animals were initially food-deprived to 85% of their free feeding body weight, but then allowed a modest growth (up to 95% of original weight) over the course of the study. Water

FR 1 schedule

Fig. 1(A–D) depicts the results of the FR 1 experiment. Each week was analyzed separately to minimize the number of factors used for the ANOVA. For week 1 (Fig. 1A), there was no significant overall effect of 6-OHDA (F(1,54)=0.007, n.s.) and no significant effect of force requirement (F(2,54)=1.54, n.s.). There was a significant difference between the weight and no-weight conditions (F(1,54)=27.00, P<0.001), and there was a significant weight/no weight×force requirement interaction (F

Discussion

In the FR 1 experiment, it was demonstrated that addition of 32, 64, and 96 g weights on the lever suppressed lever pressing. The weight/no weight×force requirement interactions, which were significant for 3 of the 4 weeks of postsurgical testing, indicate that the addition of larger weights on the levers (i.e. 64–96 g) had greater effects than addition of the smaller weight (i.e. 32 g). Injections of 6-OHDA reduced accumbens DA levels to a mean value that was approximately 8.8% of the mean

Acknowledgements

This work was supported by a grant to J.S. from the United States National Science Foundation, and by grants to M.C. from Fundacio Bancaixa-Caixa Castelló-Universitat Jaume I, Spain, and grants to S.M. from the Fulbright Foundation, and the government of Portugal.

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    Present address: Area de Psicobiologia, Campus Riu Sec, Universitat Jaume I, Castelló, Spain.

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