Effects of methamphetamine on neural responses to visual stimuli

RationaleThe behavioral and reward-related effects of stimulant drugs have been studied extensively; yet the effect of stimulants on sensory processing is still relatively unknown. Prior brain imaging studies have shown that single doses of stimulant drugs increase neural function during cognitive and attentional processes. However, it is not clear if stimulant drugs such as methamphetamine (MA) affect neural responses to novel sensory stimuli, and whether these effects depend on the visual features of the stimuli.ObjectiveIn this study, we examined the effects of a single dose of MA (20 mg oral) on neural activation in response to visual stimuli that varied on “non-straight edges” (NSE), a low-level visual feature that quantifies curved/fragmented edges and is related to perceived image complexity.MethodsHealthy adult participants (n = 18) completed two sessions in which they received MA and placebo in counterbalanced order before an fMRI scan where they viewed both high and low NSE images. Participants also completed measures of subjective drug effects throughout both sessions.ResultsDuring both sessions, high NSE images activated primary visual cortex to a greater extent than low NSE images. Further, MA increased activation only for low NSE images in three areas of visual association cortex: left fusiform, right cingulate/precuneus, and posterior right middle temporal gyrus. This interaction was unrelated to subjective drug effects.ConclusionsThese findings suggest that stimulant drugs may change the relative sensitivity of higher order sensory processing to increase visual attention when viewing less complex stimuli. Moreover, MA-induced alterations in this type of sensory processing appear to be independent of the drugs’ ability to increase feelings of well-being.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  C. Haertzen,et al.  Development of Scales Based on Patterns of Drug Effects, Using the Addiction Research Center Inventory (ARCI) , 1966, Psychological reports.

[3]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[4]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[5]  H. Engeland,et al.  Effects of methylphenidate on event-related potentials and performance of attention-deficit hyperactivity disorder children in auditory and visual selective attention tasks , 1997, Biological Psychiatry.

[6]  N. Volkow,et al.  Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. , 1999, The Journal of pharmacology and experimental therapeutics.

[7]  H. de Wit,et al.  Effects of d-amphetamine and ethanol on a measure of behavioral inhibition in humans. , 2000, Behavioral neuroscience.

[8]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[9]  H. de Wit,et al.  Effects of d-amphetamine and ethanol on a measure of behavioral inhibition in humans. , 2000, Behavioral Neuroscience.

[10]  Yu-Shin Ding,et al.  Therapeutic Doses of Oral Methylphenidate Significantly Increase Extracellular Dopamine in the Human Brain , 2001, The Journal of Neuroscience.

[11]  S. Wachtel,et al.  An fMRI Study of the Effect of Amphetamine on Brain Activity , 2001, Neuropsychopharmacology.

[12]  W. Schultz Getting Formal with Dopamine and Reward , 2002, Neuron.

[13]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[14]  J. Swanson,et al.  Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. , 2004, The American journal of psychiatry.

[15]  E. Uhlenhuth,et al.  Drug preference and mood in humans: Diazepam , 2004, Psychopharmacology.

[16]  Trevor W. Robbins,et al.  Differential effects of modafinil and methylphenidate on stop-signal reaction time task performance in the rat, and interactions with the dopamine receptor antagonist cis-flupenthixol , 2007, Psychopharmacology.

[17]  Kalanit Grill-Spector,et al.  Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex. , 2008, Journal of neurophysiology.

[18]  A. Arnsten,et al.  Toward a New Understanding of Attention-Deficit Hyperactivity Disorder Pathophysiology , 2009, CNS Drugs.

[19]  H. de Wit,et al.  The drug effects questionnaire: psychometric support across three drug types , 2012, Psychopharmacology.

[20]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[21]  Rodrigo M. Braga,et al.  Echoes of the Brain within Default Mode, Association, and Heteromodal Cortices , 2013, The Journal of Neuroscience.

[22]  Tom Hartley,et al.  Patterns of response to visual scenes are linked to the low-level properties of the image , 2014, NeuroImage.

[23]  Grigori Yourganov,et al.  The Perception of Naturalness Correlates with Low-Level Visual Features of Environmental Scenes , 2014, PloS one.

[24]  Byron Bernal,et al.  Language and Visual Perception Associations: Meta-Analytic Connectivity Modeling of Brodmann Area 37 , 2015, Behavioural neurology.

[25]  Thomas E. Nichols,et al.  Can parametric statistical methods be trusted for fMRI based group studies? , 2015, 1511.01863.

[26]  Michael C. Hout,et al.  Is the preference of natural versus man-made scenes driven by bottom–up processing of the visual features of nature? , 2015, Front. Psychol..

[27]  Nora D. Volkow,et al.  The Brain on Drugs: From Reward to Addiction , 2015, Cell.

[28]  H. Wit,et al.  Acquisition of Responses to a Methamphetamine-Associated Cue in Healthy Humans: Self-Report, Behavioral, and Psychophysiological Measures , 2015, Neuropsychopharmacology.

[29]  Omid Kardan,et al.  The order of disorder: Deconstructing visual disorder and its effect on rule-breaking. , 2016, Journal of experimental psychology. General.

[30]  Sheng Zhang,et al.  Methylphenidate Modulates Functional Network Connectivity to Enhance Attention , 2016, The Journal of Neuroscience.

[31]  L. Briars,et al.  A Review of Pharmacological Management of Attention-Deficit/Hyperactivity Disorder. , 2016, The journal of pediatric pharmacology and therapeutics : JPPT : the official journal of PPAG.

[32]  B. Waterhouse,et al.  “What have we GANEd?” A theoretical construct to explain experimental evidence for noradrenergic regulation of sensory signal processing , 2016, Behavioral and Brain Sciences.

[33]  K. Berridge,et al.  Liking, wanting, and the incentive-sensitization theory of addiction. , 2016, The American psychologist.

[34]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[35]  Dean F. Wong,et al.  The Role of Dopamine in Value-Based Attentional Orienting , 2016, Current Biology.

[36]  D. Ghahremani,et al.  The Effects of Pharmacological Opioid Blockade on Neural Measures of Drug Cue-Reactivity in Humans , 2016, Neuropsychopharmacology.

[37]  B. Waterhouse,et al.  Methylphenidate Enhances Early-Stage Sensory Processing and Rodent Performance of a Visual Signal Detection Task , 2017, Neuropsychopharmacology.

[38]  Y. Okubo,et al.  Modafinil enhances alerting-related brain activity in attention networks , 2017, Psychopharmacology.

[39]  Gang Chen,et al.  fMRI clustering and false-positive rates , 2017, Proceedings of the National Academy of Sciences.

[40]  D. Stein,et al.  Methylphenidate Enhances Grip Force and Alters Brain Connectivity , 2017, Medicine and science in sports and exercise.

[41]  S. Borgwardt,et al.  Comparative Effects of Methylphenidate, Modafinil, and MDMA on Response Inhibition Neural Networks in Healthy Subjects , 2017, The international journal of neuropsychopharmacology.

[42]  H. de Wit,et al.  Neural responses to cues paired with methamphetamine in healthy volunteers , 2018, Neuropsychopharmacology.

[43]  Marc G. Berman,et al.  A thought in the park: The influence of naturalness and low-level visual features on expressed thoughts , 2018, Cognition.