Reduced Attentional Scope in Cocaine Polydrug Users

Lorenza S. Colzato1*, Wery P. M. van den Wildenberg2, Bernhard Hommel1
1 Institute for Psychological Research & Leiden Institute for Brain and Cognition, Leiden University, Leiden, The Netherlands, 2 Amsterdam Center for the Study of Adaptive Control in Brain and Behaviour (ACACia) Psychology Department, University of Amsterdam, Amsterdam, The Netherlands
Cocaine is Europe’s second preferred recreational drug after cannabis but very little is known about possible cognitive impairments in the upcoming type of recreational cocaine user (monthly consumption). We asked whether recreational use of cocaine impacts early attentional selection processes. Cocaine-free polydrug controls (n = 18) and cocaine polydrug users (n = 18) were matched on sex, age, alcohol consumption, and IQ (using the Raven’s progressive matrices), and were tested by using the Global-Local task to measure the scope of attention. Cocaine polydrug users attended significantly more to local aspects of attended events, which fits with the idea that a reduced scope of attention may be associated with the perpetuation of the use of the drug.
Citation: Colzato LS, van den Wildenberg WPM, Hommel B (2009) Reduced Attentional Scope in Cocaine Polydrug Users. PLoS ONE 4(6): e6043. doi:10.1371/journal.pone.0006043
Editor: Antonio Verdejo García, University of Granada, Spain

Received: February 24, 2009; Accepted: May 30, 2009; Published: June 25, 2009

Copyright: © 2009 Colzato et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The research of LSC and WVDW is supported by NWO (Netherlands Organisation for Scientific Research).

Competing interests: The authors have declared that no competing interests exist.

* E-mail: colzato@fsw.leidenuniv.nl

Introduction Top

Taking cocaine by snorting route is Europe’s second preferred recreational drug habit after smoking cannabis [1]. Given the addictive properties of this psychostimulant drug, the recreational use of cocaine is a public health issue in Europe as it is in the USA [2]. It is well known that in the long term, chronic (i.e., daily) use of cocaine is associated with reduced functioning of Dopamine D2 (DAD2) receptors [3] and dysfunctions in the serotonergic and the glutaminergic system [4], [5], in lateral prefrontal cortex (LPFC), orbito-frontal cortex [6], [7], anterior cingulate, and the cerebellum [8]. Given the key role of the frontal lobe in cognitive control [9], it is thus not surprising that chronic cocaine users, compared to non-users, show a poorer ability to inhibit their overt responses [10], perform worse on tasks measuring mental flexibility [11], [12] and conflict-control [13], and show compromised ability to control their attention [14].

Only in the recent two years, some studies have systematically looked into cognitive impairments among recreational cocaine users who do not meet the criteria for abuse or dependence but take cocaine (preferably by snorting route) on a monthly frequency (1 to 4 gram). Colzato, van den Wildenberg, and Hommel [15] found that the spontaneous eyeblink rate, a marker of dopaminergic functioning [16], [but see 17], is significantly lower in recreational users than in cocaine-free controls, suggesting that even the recreational use of cocaine is associated with hypoactivity in the subcortical dopamine system. Consistent with this picture, Colzato, van den Wildenberg, and Hommel [18] observed in a stop-signal task [19] that response inhibition, but not response execution, is impaired in recreational cocaine users. Moreover, Colzato and Hommel [20] found that, relative to a sample of cocaine-free controls, recreational users show normal sensorimotor integration, but no reliable inhibition of return [21]- the (commonly robust) phenomenon of slowed responding when attention needs to return to a previously attended location [22]. While recreational cocaine users performed significantly worse than cocaine-free controls on tasks tapping cognitive flexibility, they however show comparable performance in the active maintenance and monitoring of information in working memory (WM) [23].

It is important to consider that the causal relation between cocaine use and cognitive control functions is not necessarily straightforward or linear, as pre-existent neuro-developmental factors cannot be excluded. Recent evidence showed, for instance, that monkeys having pre-existing lowered D2 receptor densities run a higher risk to use cocaine and to become addicted [24] and that chronic users may suffer pre-existing problems in inhibitory control [25] and impulsivity [26]. However, it should be noted that the connection between cocaine, DAD2 pathways, and difficulties in inhibitory control seems robust.

Whereas previous studies on recreational use of cocaine have focused on inhibitory control, “shifting” between tasks and mental sets, and the active maintenance and monitoring of information in WM, in the present study we investigated whether even earlier attentional selection processes may be affected. Considering that cocaine use is associated with impairments in the functioning of dopamine receptors, there are a number of reasons suggesting that cocaine might impact early aspects of attentional functioning. Animal models and patients studies including Parkinson’s and Huntington’s disease, schizophrenia and attention deficit hyperactivity disorder (ADHD), pathologies associated with abnormal dopaminergic levels, suggest that disturbances in attentional process (typical for those pathologies) may be modulated by dopamine (see [27] for a review).

To measure attentional selection processes, we used an adapted version of the Global-Local task developed by Navon [28], which indexes how fast people can process global and local characteristics of hierarchically constructed visual stimuli (e.g., larger letters made of smaller letters). Typically, this task gives rise to the “global precedence” effect, which means that global features can be processed faster than local features. Global precedence is supposed to reflect a bias towards a large “scope” of attention, so that a small global precedence effect would imply a reduced attentional scope. There are a number of reasons why we speculated that consuming cocaine and being exposed to it may lead, among other things, to a bias towards decreased attentional spotlight. Cocaine use is often associated with compulsive drug-seeking and drug-taking behaviors. Interestingly, it has been suggested that compulsive behavior is linked with a cognitive style focused on small details in the surroundings [29]. Moreover, it has been shown that mood affects the breadth of the attentional scope, with more positive mood leading to the processing of an increased number of peripheral stimuli [30]. Given that positive mood is assumed to temporarily increase the dopamine level [31], this implies a positive correlation between dopamine level and attentional scope. Considering that cocaine use is associated with impairments of dopamine receptors, it makes sense to assume that the attentional scope may be reduced in users. Following this reasoning, we hypothesized that cocaine polydrug users as compared to cocaine-free polydrug controls might show a less pronounced, if any, global precedence effect. Given the link between mood and dopamine, we used an affect grid [32] to check whether our results might be confounded by mood differences between the two groups.

Results Top

The two groups did not differ in mood, as indicated by the affect grid’s valence measure (Cocaine Polydrug Users: M = 5.6, Cocaine-free Polydrug Controls: M = 5.8), F(1, 34)<1, and arousal measure (Cocaine Polydrug Users: M = 5.9, Cocaine-free Polydrug Controls: M = 6.1), F(1, 34)<1.

The square roots of error percentages and median reaction times were analyzed by means of analysis of variance (ANOVA) using Target Level (global vs. local) as within- and Group (Cocaine Polydrug Users vs. Cocaine-free Polydrug Controls) as between-participants factor. The reaction time analysis showed a main effect of Target Level, F(1,34) = 79.73, p<.001, MSE = 2857.354, η2p = 0.71, which was modified by Group, F(1,34) = 7.85, p = .008, MSE = 2857.354, η2p = .19. The main effect indicated global precedence [28]: Global targets were responded to faster than local targets. However, as expected, the size of this effect varied with Group: Cocaine Polydrug Users showed a smaller, but still significant, F(1,17) = 12.26, p = .003, MSE = 4376.883, η2p = .42, global precedence effect than Cocaine-free Polydrug Controls (see Figure 1 and Table 1). Error percentages did not reveal any reliable effect, Fs(1,34)<1.60, ps>.21.