Visual responses to targets and distracters by
inferior temporal neurons after lesions of
extrastriate areas V4 and TEO
Giuseppe Bertini,
1,3,CA
Elizabeth A. Bu¡alo,
2
Peter De Weerd,
1,4
Robert Desimone
2
and Leslie G. Ungerleider
1
1
Laboratory of Brain and Cognition, NIMH, 10 Center Drive;
2
Laboratory of Neuropsychology, NIMH, 49 Convent Drive, Bethesda, MD 20892, USA
3
Present address: Department of Morphological and Biomedical Sciences, University of Verona, Strada le Grazie 8, 37134 Verona, Italy
4
Present Address: Psychology Department, Neurocognition Group, University of Maastricht, The Netherlands
CA
Corresponding Author: giuseppe.bertini@univr.it
Received 7 April 2004; accepted 20 May 2004
DOI: 10.1097/01.wnr.0000134847.86625.15
While lesions of visual areas V4 and TEO only modestly a¡ect dis-
crimination of isolated objects, they signi¢cantly impair the ability
to selectively attend to an object surrounded by distracters.To test
whether such de¢cits result from a loss of inputs to higher order
areas, we recorded from area TE neurons after removing portions
of V4 and TEO in a monkey. Responses to isolated targets in a le-
sion-a¡ected visual quadrant were substantially preserved, indicat-
ing that TE still receives information even after removing a major
source of input. Distracters increased or decreased the response
to targets more in the lesion-a¡ected than in the normal quadrant,
supporting the idea that V4 and/orTEO are sites where top-down
attentional inputs ¢lter out distracting stimuli. NeuroReport
15:1611^1615 c 2004 Lippincott Williams & Wilkins.
Key words: Attention; Electrophysiology; Receptive ¢eld; Rhesus monkey; Visual cortex; Visual perception
INTRODUCTION
When attention is focused on a behaviorally relevant
stimulus in the visual field, the processing of that object is
enhanced relative to that of any surrounding distracters.
Several electrophysiological studies have suggested that this
comes about by the filtering of distracting stimuli from the
receptive fields of neurons along the ventral processing
stream, an occipitotemporal cortical pathway that is critical
for visual object recognition in primates [1–4].
The important role of ventral stream areas in attentional
filtering is also supported by several lesion studies [5–11]. In
particular, De Weerd et al. [9,11] found that lesions of
extrastriate areas V4 and/or TEO produced a severe impair-
ment in the discrimination of a variety of target stimuli when
they were surrounded by salient luminance distracters,
whereas the discrimination of the same stimuli posed little
difficulty in the absence of distracters. Similar results have
been found in a human patient with a V4 lesion [12].
Because areas V4 and TEO provide the main input to
inferior temporal area TE, the next processing stage in the
ventral stream [13,14], one possible explanation for the
behavioral results is that V4 and TEO lesions simply deprive
TE of visual input, essentially deafferenting the highest
levels of the ventral stream. In that case, object discrimina-
tion might be mediated by alternative pathways that do not
have the capacity to both process object features and filter
out distracting stimuli from receptive fields. To test this, we
recorded the responses of area TE neurons to target stimuli
presented either in a visual quadrant affected by a combined
V4 and TEO lesion, or in an unaffected quadrant.
If TE neurons did continue to respond to visual input in
the absence of V4 and TEO, the next step would be to test
whether the TE neurons would show reduced efficiency in
filtering out distracting information from their receptive
fields. We planned to test this by comparing neuronal
responses in the normal and lesion-affected quadrants to
stimuli presented either alone or surrounded by irrelevant
distracters (Fig. 1d). We reasoned that if V4 and TEO were
critical sites where top-down attentional inputs filtered
distracters from receptive fields, then lesions of these areas
would result in impaired attentional filtering by neurons in
area TE, which receives inputs from these two areas.
MATERIALS AND METHODS
Lesions and recording procedure: One adult male monkey
(Macaca mulatta, monkey M1 from ref. [9]), weighing B9 kg,
was used. All surgical and behavioral procedures were
carried out in accordance with National Institutes of Health
guidelines, under a protocol approved by the National
Institute of Mental Health Institutional Animal Care
and Use Committee, and have been described in detail
VISION, CENTRAL NEUROREPORT
0959-4965 c Lippincott Williams & Wilkins Vol 15 No 10 19 July 2004 1611
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.