Download Perception, Memory, and Action in Frontal and Parietal Cortex

J Neurophysiol 95: 3309 –3310, 2006;
doi:10.1152/jn.00163.2006.
Editorial Focus
Perception, Memory, and Action in Frontal and Parietal Cortex. Focus on
“Selection and Maintenance of Saccade Goals in the Human Frontal
Eye Fields”
Vincent P. Ferrera and Jack Grinband
Mahoney Center for Brain and Behavior, Center for Neurobiology and Behavior, Department of Psychiatry, Columbia University and New
York State Psychiatric Institute, New York, New York
Address for reprint requests and other correspondence: V. Ferrera, Mahoney
Center for Brain and Behavior, Center for Neurobiology and Behavior,
Department of Psychiatry, Columbia University, New York, NY (E-mail:
[email protected]).
www.jn.org
response. A previous study (Connolly et al. 2002) showed that
motor set modulated activity in FEF but not IPS.
Other interpretations are possible, but the most likely of
these are ruled out by the data. For example, one can imagine
that during the first delay, subjects covertly prepare all four
movements instead of (or in addition to) simply remembering
the stimulus locations. In this case, one might infer that IPS is
more closely involved in movement planning because it has the
greatest activation during the first delay. This explanation can
be rejected because IPS activation fell to baseline levels during
the second delay despite the continued need for motor response
preparation. FEF activation remained significantly above baseline. A reduction in the number of planned movements from
four to one might account for the reduced activation seen in
both FEF and IPS but not the observed inversion in the relative
strength of activation between the two areas.
The fact that the number of locations to be remembered
changes once the target is cued raises the issue of whether an
overall reduction in the level of BOLD activation between the
first and second delays is due to response selection, per se, as
opposed to the corresponding reduction in memory load. To
address this, Curtis and D’Esposito looked for lateralized
activation in IPS and FEF. It is well known that the majority of
neurons in the parietal and prefrontal cortex prefer contralateral
stimuli and/or contraversive movements (Blatt et al. 1990;
Funahashi et al. 1990). Because the initial stimulus array
covered both visual hemifields, the first delay interval showed
bilateral brain activity that was equal across the two hemispheres. However, after presenting the target cue, activity in
the second delay interval became strongly lateralized in the
hemisphere contralateral to the position of the target. The
lateralized IPS activation was short-lived, but FEF activation
was sustained and the degree of lateralization increased over
time until the response was executed. Thus the lateralization of
activity in FEF increased even though there was only a single
item in memory. More importantly, lateralized FEF activation
just prior to the motor response predicted the direction of the
eye movement; IPS activation did not.
Neurophysiological studies in monkey FEF and LIP support
the visual-motor distinction. These studies have revealed neurons with visual, movement and mixed visual-movement activity (Andersen et al. 1990; Barash et al. 1991; Bruce and
Goldberg 1985). Visual and visual-movement neurons are
found in both areas (Chafee and Goldman-Rakic 1998); however, pure movement neurons without visual responses are
common in FEF but rare in LIP. Movement-related activity in
parietal cortex tends to evolve slowly and is best demonstrated
in delayed-response tasks. If monkeys are required to make an
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3309
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Visually guided behavior engages posterior parietal and
lateral prefrontal cortex, yet the unique contributions of these
brain regions are strongly contested. Recent experiments by
Curtis and D’Esposito use functional magnetic resonance imaging to differentiate the roles of parietal and prefrontal cortex
with respect to visual working memory and movement planning.
The notion of functional specialization in the visual system
has a long if not uncontroversial history (Goodale and Milner
1992; Scheider 1969; Trevarthen 1968; Ungerleider and Mishkin 1982). One current area of contention is the division of
labor between posterior parietal (PPC) and lateral prefrontal
cortex (PFC). Both are involved in visual-motor transformations, but is one inherently more “visual” and the other more
“motor”? In this issue of Journal of Neurophysiology (p.
3923–3927), a functional imaging study by Curtis and
D’Esposito (2006) shows that PPC and PFC perform a kind of
dance during visual-motor behavior with first one area taking
the lead and then the other. Their results suggest that PPC is
more active during the encoding and storage of visual stimuli
in working memory, but PFC becomes more active during
response preparation and execution. These results lend support
to the view that parietal cortex contains a general purpose
visual map (Gottlieb et al. 1998), whereas prefrontal cortex is
more action oriented.
Curtis and D’Esposito’s experiment used a delayed-response
task that evoked activity in a region of the precentral sulcus
likely to be the human frontal eye field (FEF), and a region in
the intraparietal sulcus (IPS) likely to be the human equivalent
of monkey lateral intraparietal area (LIP). Subjects were required to remember an array of four stimulus locations during
an extended delay period. At the end of this delay, a cue
identified one of the four locations as the saccadic goal. A
second delay interval required the maintenance of the target
location until a movement execution cue was given. IPS and
FEF showed opposite patterns of blood-oxygen-level-dependent (BOLD) activitation during the two delay intervals. During the “visual memory” delay, activation was stronger in IPS
than in FEF. However, during the “movement preparation”
delay, the pattern of activation reversed. These results support
the idea that neural activity in IPS is primarily influenced by
the processing and storage of visual stimuli, whereas FEF is
more heavily recruited during the preparation of the motor
Editorial Focus
3310
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immediate “anti-saccade” (a saccade directed away from the
visual stimulus) when a target appears, FEF neurons are able to
reliably signal the direction of the movement (Everling and
Munoz 2000), but LIP neurons are not (Gottlieb et al. 1999).
Finally, whereas eye movements can be elicited by stimulating
either FEF or LIP, stimulation thresholds in FEF are much
lower than LIP (Bruce et al. 1985; Shibutani et al. 1984).
FEF and LIP are key components of a fronto-parietal network that is involved in spatial attention, working memory, and
eye movements (Posner and Petersen 1990). Different labs
have come to almost diametrically opposed views on the role
of parietal cortex in this circuit. One group has proposed that
parietal cortex represents the attentional salience of visual
objects (Goldberg et al. 2002), whereas others have emphasized its role in motor planning (Snyder et al. 2000). The view
that FEF is primarily “motor” has likewise been called into
question by studies showing the involvement of FEF in attentional tasks (Moore et al. 2003; Thompson et al. 2005). Electrophysiologically, FEF and IPS show as many similarities as
differences. The value of the Curtis and D’Esposito study is
that it clearly shows, at the level of fMRI, a movement
planning signal in FEF that is not present in IPS, thus providing
evidence for functional specialization in the fronto-parietal
circuit.