Research Report
Putamen neurons process both sensory and motor information
during a complex task
Ana F. Vicente
a
, Maria A. Bermudez
a,
⁎
, Maria del Carmen Romero
a
,
Rogelio Perez
b
, Francisco Gonzalez
a, c
a
CIMUS (Department of Physiology), University of Santiago de Compostela, Av. Barcelona s/n, E-15706 Santiago de Compostela, Spain
b
Department of Ophthalmology, Hospital da Barbanza, Ribeira, E-15993 A Coruña, Spain
c
Department of Ophthalmology, University Hospital, Santiago de Compostela, E-15706, Spain
ARTICLE INFO ABSTRACT
Article history:
Accepted 18 May 2012
Available online 25 May 2012
The putamen has classically been considered to be primarily a motor structure. It is
involved in a broad range of roles and its neurons have been postulated to function as
pattern classifiers of behaviourally significant events. However, its specific role in motor
and sensory processing is still unclear. For the purpose of better categorizing putamen
neurons, we trained two rhesus monkeys to perform multisensory operant tasks by using
complex stimuli such as short videoclips. Trials involved image or soundtrack or both.
Some stimuli required a motor response associated to reward, whereas others did not
require response and produced no reward. We found that neurons in the putamen showed
pure visual responses, action-related activity, and reward responses. Insofar as action-
related activity, preparation of movement, movement execution, and withholding of
movement involved three different putamen neuron populations. Moreover, our data
suggest an involvement of putamen neurons in processing primary rewards and visual
events in a complex task, which may contribute to reinforcement learning through
stimulus–reward association.
© 2012 Elsevier B.V. All rights reserved.
Keywords:
Putamen
Motor activity
Reward
Visual
Withholding of movement
1. Introduction
Several studies have shown that the putamen together with
the caudate is the major input structures of the basal ganglia.
The putamen receives connections from cortical areas, the
thalamus, and the midbrain. In turn, it sends connections to
other components of the basal ganglia such as globus
pallidus and substantia nigra (DeLong, 2000; Galvan et al.,
2006; Utter and Basso, 2008). Traditionally, neurons from the
putamen nucleus have been related to the execution of
movement (Jaeger et al., 1995; Tolkunov et al., 1998; Ueda and
Kimura, 2003). However, considerable evidence also suggests
its role in learning processes as shown by reward delivery
activation (Cromwell et al., 2005; Graybiel, 1995; Lau and
Glimcher, 2007) or activation by stimuli that anticipate the
reward onset (Blazquez et al., 2002; Kimura et al., 2003; Ravel
et al., 2003). Finally, recent studies suggest an involvement of
the putamen in the processing of visual information (Romero
et al., 2008).
Motor-related activity in the putamen has conventionally
been studied by using operant tasks in which animals need to
learn associations between certain stimuli and a particular
BRAIN RESEARCH 1466 (2012) 70 – 81
⁎ Corresponding author at: CIMUS (Department of Physiology), University of Santiago de Compostela, Avda. Barcelona s/n, Santiago de
Compostela 15706, Spain. Fax: +34 981574145.
E-mail address: maria.bermudez@usc.es (M.A. Bermudez).
0006-8993/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.brainres.2012.05.037
Available online at www.sciencedirect.com
www.elsevier.com/locate/brainres