Elsevier

Behavioural Brain Research

Volume 175, Issue 1, 25 November 2006, Pages 75-81
Behavioural Brain Research

Research report
Relationship of delay aversion and response inhibition to extinction learning, aggression, and sexual behaviour

https://doi.org/10.1016/j.bbr.2006.08.003Get rights and content

Abstract

Impulsivity is an important symptom of many psychiatric disorders, and can be divided into two subtypes: response inhibition deficits and delay aversion. In the present study, we investigated the relationship between delay aversion and response inhibition, both to each other and to locomotion, extinction of conditioned responses, sexual behaviour, and aggressive behaviour. To that end, we quantified the behaviour of 24 rats in several tests. To measure response inhibition, rats were trained in a stop-signal task. In this operant task, rats were rewarded food if they inhibited execution of a response after presentation of an audible stop-signal. Delay aversion was measured in an operant task in which rats made a choice between a small, immediately available reward and a large reward available after a delay. The results showed that delay aversion and response inhibition were independent. Responses during extinction and various measures of aggressive behaviour were positively correlated to delay aversion. The speed of go-trials in the stop-task was correlated to non-aggressive behaviour. We conclude that the role of response inhibition in various behaviours is small, but delay aversion in particular contributes to several other behaviours, such as aggressive behaviour and extinction.

Introduction

Some situations call for rapid responding based on little information, and people and animals are well equipped for such situations. However, if this rapid responding is applied to situations where forethought is required, behaviour may become impulsive and may seriously hamper everyday life [1]. Recent research suggests that at least two different processes may lead to impulsive behaviour [2]. Delay aversion is the first process leading to impulsivity. Impulsive individuals perceive delays as especially aversive, and therefore make decisions resulting in immediate gratification, or, if delays are unavoidable, avert attention from the long-term goal to decrease the subjective delay [3], [4], [5], [6]. Intolerance to delayed rewards may be the result of alterations in the frontostriatal reward networks, including the nucleus accumbens core [7], [8]. In the second theory, impulsivity is the result of a failure to inhibit ongoing or planned responses [9]. This process is often described as a competition between hypothetical go- and stop-signals in which the winning signal determines whether or not a response is made [the horse-race model: 10]. Frontal and medial striatal areas are implicated in inhibiting prepotent responses [8], [11], [12].

The two impulsivity subtypes are core symptoms of many psychiatric disorders. In preschool children suffering from attention-deficit hyperactivity disorder (ADHD), delay aversion is especially prominent, occurring alone in 27% of the children, and in 29% together with a response inhibition deficit [13], [14]. Further, heroin and cocaine abusers display delay aversion [15], [16], and a similar delay aversion is seen in smokers [17], [18] and alcoholics [19]. Delay aversion is not just associated with addiction to drugs, as it predicts pathological gambling severity as well [20], [21], suggesting that it is not the drugs causing changes in delay tolerance, but rather the trait causing susceptibility to addiction. Furthermore, a recent study showed that delay aversion predicts the acquisition of cocaine self-administration in rats [22]. A shared underlying core deficit may also explain the high incidence of comorbid ADHD and substance-abuse disorders [23], [24]. An association has also been found between delay aversion and classroom observations of aggressive behaviour [4]. However, the association between delay aversion and aggression has not yet been extensively studied.

Response inhibition also plays a central role in ADHD, occurring alone in 15% of preschool patients and together with delay aversion in another 29% [13], [14]. The response inhibition deficit in ADHD patients is well studied across all ages, including adults [25], [26], [27]. Other disorders in which response inhibition plays an important role are oppositional defiant disorder (ODD) and conduct disorder (CD) [28], [29]. Descriptions of impulsive aggression (such as ‘hair-trigger’ [30]) suggest an inability to inhibit aggressive urges and thus a potential involvement of response inhibition.

Clearly, both delay aversion and response inhibition are central traits important to many behaviours, both normal and pathological. Before the two impulsivity subtypes were recognized as complementary, many studies were aimed at reinforcing one theory as the main or core symptom of a disorder [3], [9]. Now that delay aversion and response inhibition are perceived as independent contributors to impulsivity, studies have focused on finding differences and similarities between the two subtypes [2], [5], [13], and determination of the relative contributions of both impulsivity subtypes to pathological behaviour [4]. A disadvantage of the groups used in those studies is their heterogeneity. The variability within children diagnosed with ADHD can be very large, in part because both impulsivity subtypes can lead to ADHD symptoms [31].

The aim of the present study is to determine the relationship between delay aversion and response inhibition and their involvement in various other basal behaviours. To that end, we quantified the behaviours of 24 untreated rats in a number of different tests. This approach can uniquely be used to determine the overlap between the two impulsivity subtypes because the experimental group is very homogeneous compared to human samples. Further, near-absolute control can be executed over the environment of the animals. Therefore, any associations are likely to be the result of actual overlap between the two impulsivity constructs. Finally, the influence of the two impulsivity subtypes on a number of other basal behaviours important for animal survival can reliably be measured.

Section snippets

Animals and housing

Twenty-four male Wistar rats (HsdCpb:WU) obtained from Harlan (The Netherlands) weighing 125 g on arrival, were housed in a light (lights on from 7:00 to 19:00), temperature (21 ± 2 °C), and humidity (50 ± 10%) controlled animal facility. At the start of the study, they were housed in groups of four male rats. At this stage, animals received 15 g/day/rat of standard laboratory chow and free water. This food restriction served as an incentive for responding in the operant tasks (the stop-signal task,

Results

As is clear from Fig. 1 neither the speed of the stop-process nor the speed of the go-process is related to delay aversion. Neither the SSRT nor the mRT were correlated with the AUPC (r = 0.06, NS and r = 0.08, NS, respectively). Similar findings are reported in humans [13], [14], although in some reports go response time is mildly correlated to inhibition in a delayed reward task [4].

The correlations between the measures of impulsivity and the remaining measures are listed in Table 1. The speeds

Discussion

The present article shows that response inhibition is unrelated to delay aversion in a homogeneous group of rats. In children, a similar lack of association has been reported in several studies. Dalen et al. [13] found a lack of association in 3-year-old children tested on a delay aversion task (in which subjects could choose between one sweet delivered after 1 s or two sweets delivered after 17 s) and a go–no go inhibition task. Sonuga-Barke et al. [14] have shown that response inhibition

Acknowledgement

We are grateful to Wim van der Wal for performing the testosterone determinations.

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