title: Oscillatory activity in the medial prefrontal cortex and nucleus accumbens correlates with impulsivity and reward outcome.
abstract: Actions expressed prematurely without regard for their consequences are considered impulsive. Such behaviour is governed by a network of brain regions including the prefrontal cortex (PFC) and nucleus accumbens (NAcb) and is prevalent in disorders including attention deficit hyperactivity disorder (ADHD) and drug addiction. However, little is known of the relationship between neural activity in these regions and specific forms of impulsive behaviour. In the present study we investigated local field potential (LFP) oscillations in distinct sub-regions of the PFC and NAcb on a 5-choice serial reaction time task (5-CSRTT), which measures sustained, spatially-divided visual attention and action restraint. The main findings show that power in gamma frequency (50-60 Hz) LFP oscillations transiently increases in the PFC and NAcb during both the anticipation of a cue signalling the spatial location of a nose-poke response and again following correct responses. Gamma oscillations were coupled to low-frequency delta oscillations in both regions; this coupling strengthened specifically when an error response was made. Theta (7-9 Hz) LFP power in the PFC and NAcb increased during the waiting period and was also related to response outcome. Additionally, both gamma and theta power were significantly affected by upcoming premature responses as rats waited for the visual cue to respond. In a subgroup of rats showing persistently high levels of impulsivity we found that impulsivity was associated with increased error signals following a nose-poke response, as well as reduced signals of previous trial outcome during the waiting period. Collectively, these in-vivo neurophysiological findings further implicate the PFC and NAcb in anticipatory impulsive responses and provide evidence that abnormalities in the encoding of rewarding outcomes may underlie trait-like impulsive behaviour.
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Nicholas A
authors.initials: NA
authors.lastname: Donnelly
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Tahl
authors.initials: T
authors.lastname: Holtzman
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom; Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, Virginia, United States of America.
authors.forename: P Dylan
authors.initials: PD
authors.lastname: Rich
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom; Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.
authors.forename: Alejo J
authors.initials: AJ
authors.lastname: Nevado-Holgado
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom; Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.
authors.forename: Anushka B P
authors.initials: AB
authors.lastname: Fernando
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Gert
authors.initials: G
authors.lastname: Van Dijck
authors.affiliation: Department of Microsystems Engineering, Microsystem Materials Laboratory, University of Freiburg, Freiburg, Germany.
authors.forename: Tobias
authors.initials: T
authors.lastname: Holzhammer
authors.affiliation: Department of Microsystems Engineering, Microsystem Materials Laboratory, University of Freiburg, Freiburg, Germany.
authors.forename: Oliver
authors.initials: O
authors.lastname: Paul
authors.affiliation: Department of Microsystems Engineering, Microsystem Materials Laboratory, University of Freiburg, Freiburg, Germany.
authors.forename: Patrick
authors.initials: P
authors.lastname: Ruther
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Ole
authors.initials: O
authors.lastname: Paulsen
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Trevor W
authors.initials: TW
authors.lastname: Robbins
authors.affiliation: Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdom; Department of Psychology, University of Cambridge, Cambridge, United Kingdom; Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.
authors.forename: Jeffrey W
authors.initials: JW
authors.lastname: Dalley
mesh_terms: D000818:Animals; D001289:Attention Deficit Disorder with Hyperactivity / Q000503:physiopathology*; D002755:Choice Behavior / Q000502:physiology*; D006801:Humans; D007175:Impulsive Behavior / Q000502:physiology*; D008297:Male; D009043:Motor Activity / Q000502:physiology; D009714:Nucleus Accumbens / Q000502:physiology; D017397:Prefrontal Cortex / Q000502:physiology*; D051381:Rats; D011930:Reaction Time; D012201:Reward