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      Impulsive choice in hippocampal but not orbitofrontal cortex-lesioned rats on a nonspatial decision-making maze task

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          Abstract

          Orbitofrontal cortical (OFC) and hippocampal (HPC) lesions in primates and rodents have been associated with impulsive behaviour. We showed previously that OFC- or HPC-lesioned rats chose the immediate low-reward (LR) option in preference to the delayed high-reward (HR) option, where LR and HR were associated with different spatial responses in a uniform grey T-maze. We now report that on a novel nonspatial T-maze task in which the HR and LR options are associated with patterned goal arms (black-and-white stripes vs. gray), OFC-lesioned rats did not show impulsive behaviour, choosing the delayed HR option, and were indistinguishable from controls. In contrast, HPC-lesioned rats exhibited impulsive choice in the nonspatial decision-making task, although they chose the HR option on the majority of trials when there was a 10-s delay associated with both goal arms. The previously reported impairment in OFC-lesioned rats on the spatial version of the intertemporal choice task is unlikely to reflect a general problem with spatial learning, because OFC lesions were without effect on acquisition of the standard reference memory water-maze task and spatial working memory performance (nonmatching-to-place) on the T-maze. The differential effect of OFC lesions on the two versions of the intertemporal choice task may be explained instead in terms of the putative role of OFC in using associative information to represent expected outcomes and generate predictions. The impulsivity in HPC-lesioned rats may reflect impaired temporal information processing, and emphasizes a role for the hippocampus beyond the spatial domain.

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          Most cited references45

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          What makes us tick? Functional and neural mechanisms of interval timing.

          Time is a fundamental dimension of life. It is crucial for decisions about quantity, speed of movement and rate of return, as well as for motor control in walking, speech, playing or appreciating music, and participating in sports. Traditionally, the way in which time is perceived, represented and estimated has been explained using a pacemaker-accumulator model that is not only straightforward, but also surprisingly powerful in explaining behavioural and biological data. However, recent advances have challenged this traditional view. It is now proposed that the brain represents time in a distributed manner and tells the time by detecting the coincidental activation of different neural populations.
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            Frontal-subcortical circuits and human behavior.

            This synthetic review was performed to demonstrate the utility of frontal-subcortical circuits in the explanation of a wide range of human behavioral disorders. Reports of patients with degenerative disorders or focal lesions involving frontal lobe or linked subcortical structures were chosen from the English literature. Individual case reports and group investigations from peer-reviewed journals were evaluated. Studies were included if they described patient behavior in detail or reported pertinent neuropsy-chological findings and had compelling evidence of a disorder affecting frontal-subcortical circuits. Information was used if the report from which it was taken met study selection criteria. Five parallel segregated circuits link the frontal lobe and subcortical structures. Clinical syndromes observed with frontal lobe injury are recapitulated with lesions of subcortical member structures of the circuits. Each prefrontal circuit has a signature behavioral syndrome: executive function deficits occur with lesions of the dorsolateral prefrontal circuit, disinhibition with lesions of the orbitofrontal circuit, and apathy with injury to the anterior cingulate circuit. Depression, mania, and obsessive-compulsive disorder may also be mediated by frontal-subcotical circuits. Movement disorders identify involvement of the basal ganglia component of frontal-subcortical circuits. Frontal-subcortical circuits mediate many aspects of human behavior.
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              Dissociation in prefrontal cortex of affective and attentional shifts.

              The prefrontal cortex is implicated in such human characteristics as volition, planning, abstract reasoning and affect. Frontal-lobe damage can cause disinhibition such that the behaviour of a subject is guided by previously acquired responses that are inappropriate to the current situation. Here we demonstrate that disinhibition, or a loss of inhibitory control, can be selective for particular cognitive functions and that different regions of the prefrontal cortex provide inhibitory control in different aspects of cognitive processing. Thus, whereas damage to the lateral prefrontal cortex (Brodmann's area 9) in monkeys causes a loss of inhibitory control in attentional selection, damage to the orbito-frontal cortex in monkeys causes a loss of inhibitory control in 'affective' processing, thereby impairing the ability to alter behaviour in response to fluctuations in the emotional significance of stimuli. These findings not only support the view that the prefrontal cortex has multiple functions, but also provide evidence for the distribution of different cognitive functions within specific regions of prefrontal cortex.

                Author and article information

                Journal
                Eur J Neurosci
                ejn
                The European Journal of Neuroscience
                Blackwell Publishing Ltd
                0953-816X
                1460-9568
                August 2009
                : 30
                : 3
                : 472-484
                Affiliations
                simpleDepartment of Experimental Psychology, University of Oxford South Parks Road, Oxford, OX1 3UD, UK
                Author notes
                Correspondence: Dr D. M. Bannerman or Dr T. G. Campbell, as above. E-mail: david.bannerman@ 123456psy.ox.ac.uk or thomas.campbell@ 123456psy.ox.ac.uk
                [*]

                Joint first authors: T.Y.M and D.M.B contributed equally to this manuscript.

                Article
                10.1111/j.1460-9568.2009.06837.x
                2777256
                19656177
                f0f6888d-a8f9-4ebb-a445-296082394d16
                Journal compilation © 2009 Federation of European Neuroscience Societies and Blackwell Publishing Ltd

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 07 November 2008
                : 10 June 2009
                : 10 June 2009
                Categories
                Behavioral Neuroscience

                Neurosciences
                delay discounting,reversal,water maze,spatial,t-maze
                Neurosciences
                delay discounting, reversal, water maze, spatial, t-maze

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