Cingulate neglect in humans: Disruption of contralesional reward learning in right brain damage

Francesca Lecce, Francesca Rotondaro, Sonia Bonnì, Augusto Carlesimo, Michel Thiebaut de Schotten, Francesco Tomaiuolo, Fabrizio Doricchi
Cortex. 2015-01-01; 62: 73-88
DOI: 10.1016/j.cortex.2014.08.008

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1. Cortex. 2015 Jan;62:73-88. doi: 10.1016/j.cortex.2014.08.008. Epub 2014 Aug 27.

Cingulate neglect in humans: disruption of contralesional reward learning in
right brain damage.

Lecce F(1), Rotondaro F(2), Bonnì S(3), Carlesimo A(4), Thiebaut de Schotten
M(5), Tomaiuolo F(6), Doricchi F(7).

Author information:
(1)Fondazione Santa Lucia IRCCS, Roma, Italy; Institute of Cognitive
Neuroscience, University College London, London, UK.
(2)Fondazione Santa Lucia IRCCS, Roma, Italy; Dipartimento di Psicologia 39,
Università degli Studi di Roma ‘La Sapienza’, Roma, Italy.
(3)Fondazione Santa Lucia IRCCS, Roma, Italy.
(4)Fondazione Santa Lucia IRCCS, Roma, Italy; Dipartimento di Medicina dei
Sistemi, Universita’ Tor Vergata, Roma, Italy.
(5)Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute
of Psychiatry, King’s College London, London, UK; CNRS, UMR 7225, INSERM-UPMC
UMR_S 1127, Centre de Recherche de l’Institut du Cerveau et de la Moelle
épinière, Brain and Spine Institute, Paris, France.
(6)Auxilium Vitae, Volterra, Pisa, Italy.
(7)Fondazione Santa Lucia IRCCS, Roma, Italy; Dipartimento di Psicologia 39,
Università degli Studi di Roma ‘La Sapienza’, Roma, Italy. Electronic address:

Motivational valence plays a key role in orienting spatial attention.
Nonetheless, clinical documentation and understanding of motivationally based
deficits of spatial orienting in the human is limited. Here in a series of one
group-study and two single-case studies, we have examined right brain damaged
patients (RBD) with and without left spatial neglect in a spatial reward-learning
task, in which the motivational valence of the left contralesional and the right
ipsilesional space was contrasted. In each trial two visual boxes were presented,
one to the left and one to the right of central fixation. In one session monetary
rewards were released more frequently in the box on the left side (75% of trials)
whereas in another session they were released more frequently on the right side.
In each trial patients were required to: 1) point to each one of the two boxes;
2) choose one of the boxes for obtaining monetary reward; 3) report explicitly
the position of reward and whether this position matched or not the original
choice. Despite defective spontaneous allocation of attention toward the
contralesional space, RBD patients with left spatial neglect showed preserved
contralesional reward learning, i.e., comparable to ipsilesional learning and to
reward learning displayed by patients without neglect. A notable exception in the
group of neglect patients was L.R., who showed no sign of contralesional reward
learning in a series of 120 consecutive trials despite being able of reaching
learning criterion in only 20 trials in the ipsilesional space. L.R. suffered a
cortical-subcortical brain damage affecting the anterior components of the
parietal-frontal attentional network and, compared with all other neglect and
non-neglect patients, had additional lesion involvement of the medial anterior
cingulate cortex (ACC) and of the adjacent sectors of the corpus callosum. In
contrast to his lateralized motivational learning deficit, L.R. had no lateral
bias in the early phases of attentional processing as he suffered no
contralesional visual or auditory extinction on double simultaneous
tachistoscopic and dichotic stimulation and detected, with no exception, single
contralesional visual and auditory stimuli. In a separate study, we were able to
compare L.R. with another RBD patient, G.P., who had a selective lesion in the
right ACC, in the adjacent callosal connections and the medial-basal prefrontal
cortex. G.P. had no contralesional neglect and displayed normal reward learning
both in the left and right side of space. These findings show that contralesional
reward learning is generally preserved in RBD patients with left spatial neglect
and that this can be exploited in rehabilitation protocols. Contralesional reward
learning is severely disrupted in neglect patients when an additional lesion of
the ACC is present: however, as demonstrated by the comparison between L.R. and
G.P. cases, selective unilateral lesion of the right ACC does not produce
motivational neglect for the contralesional space.

Copyright © 2014 Elsevier Ltd. All rights reserved.

DOI: 10.1016/j.cortex.2014.08.008
PMID: 25239855 [Indexed for MEDLINE]

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