Adaptive aspects of impulsivity and interactions with effects of catecholaminergic agents in the 5-choice serial reaction time task: implications for ADHD

Chiara Toschi,Ulrik Gether,Maximilian G Parker,Trevor W Robbins,Parisa Moazen,Mona El-Sayed Hervig,Jeffrey W Dalley

doi:10.1007/s00213-021-05883-y

Chiara Toschi, Ulrik Gether + Show 5 more

Open Access

https://doi.org/10.1007/s00213-021-05883-y

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Abstract

BackgroundWork in humans has shown that impulsivity can be advantageous in certain settings. However, evidence for so-called functional impulsivity is lacking in experimental animals.AimsThis study investigated the contexts in which high impulsive (HI) rats show an advantage in performance compared with mid- (MI) and low impulsive (LI) rats. We also assessed the effects of dopaminergic and noradrenergic agents to investigate underlying neurotransmitter mechanisms.MethodsWe tested rats on a variable inter-trial interval (ITI) version of the 5-choice serial reaction time task (5CSRTT). Rats received systemic injections of methylphenidate (MPH, 1 mg/kg and 3 mg/kg), atomoxetine (ATO, 0.3 mg/kg and 1 mg/kg), amphetamine (AMPH, 0.2 mg/kg), the alpha-2a adrenoceptor antagonist atipamezole (ATI, 0.3 mg/kg) and the alpha-1 adrenoceptor agonist phenylephrine (PHEN, 1 mg/kg) prior to behavioural testing.ResultsUnlike LI rats, HI rats exhibited superior performance, earning more reinforcers, on short ITI trials, when the task required rapid responding. MPH, AMPH and ATI improved performance on short ITI trials and increased impulsivity in long ITI trials, recapitulating the behavioural profile of HI. In contrast, ATO and PHEN impaired performance on short ITI trials and decreased impulsivity, thus mimicking the behavioural profile of LI rats. The effects of ATO were greater on MI rats and LI rats.ConclusionsThese findings indicate that impulsivity can be advantageous when rapid focusing and actions are required, an effect that may depend on increased dopamine neurotransmission. Conversely, activation of the noradrenergic system, with ATO and PHEN, led to a general inhibition of responding.

Highlights

Chiara Toschi and Mona El-Sayed Hervig contributed to this work.Impulsivity is a multifactorial construct more generally understood as the tendency to act prematurely without foresight (Dalley et al 2011; Evenden 1999; Whiteside and Lynam 2001; Winstanley et al 2006)
To further test how performance on rapid trials was affected by context and the extent to which high impulsive (HI) and low impulsive (LI) rats adapt to high-event rate trials, we evaluated the effects of short trial presentations, with pseudo-randomly interleaved 3 s and 2 s inter-trial interval (ITI)
Impulsivity phenotype determined the efficacy of performance in terms of earned reinforcers at different ITI values for the second day of testing

Summary

Introduction

Impulsivity is a multifactorial construct more generally understood as the tendency to act prematurely without foresight (Dalley et al 2011; Evenden 1999; Whiteside and Lynam 2001; Winstanley et al 2006) It is often regarded as a maladaptive trait and is widely associated with various psychiatric disorders, including drug addiction (de Wit 2009; Jentsch and Taylor 1999; Kollins et al 2005) and attentiondeficit hyperactivity disorder (ADHD, Solanto 2002). When there is little time available to make a decision, high impulsive individuals respond with greater accuracy than low impulsive individuals (Dickman and Meyer 1988). In line with this early evidence, it was recently shown that trait impulsivity boosts performance in highly rewarding settings (Cools et al 2005). We assessed the effects of dopaminergic and noradrenergic agents to investigate underlying neurotransmitter mechanisms

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