Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

Anderson, John C.; Kennedy, Henry; Martin, Kevan A

doi:10.1523/jneurosci.0622-11.2011

Cited by 102 publications

(114 citation statements)

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“…In the present study, in addition to the amygdala, we selected ROIs in the ventral visual pathway (from V1 to area TE), which respond selectively to visual features relevant for object identification, such as color, shape, and texture (27). We also investigated the effects of OT on brain activity in FEF and LIP, which are heavily interconnected and important for visual attention (28). Finally, we examined OT's modulatory effects on three subregions of the PFC: DLPFC, VLPFC, and OFC (29), which are areas known to play important roles in emotion-related cognitive behavior.…”

Section: Discussionmentioning

confidence: 99%

Oxytocin modulates fMRI responses to facial expression in macaques

Liu¹,

Hadj-Bouziane²,

Jones³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Increasing evidence has shown that oxytocin (OT), a mammalian hormone, modifies the way social stimuli are perceived and the way they affect behavior. Thus, OT may serve as a treatment for psychiatric disorders, many of which are characterized by dysfunctional social behavior. To explore the neural mechanisms mediating the effects of OT in macaque monkeys, we investigated whether OT would modulate functional magnetic resonance imaging (fMRI) responses in face-responsive regions (faces vs. blank screen) evoked by the perception of various facial expressions (neutral, fearful, aggressive, and appeasing). In the placebo condition, we found significantly increased activation for emotional (mainly fearful and appeasing) faces compared with neutral faces across the faceresponsive regions. OT selectively, and differentially, altered fMRI responses to emotional expressions, significantly reducing responses to both fearful and aggressive faces in face-responsive regions while leaving responses to appeasing as well as neutral faces unchanged. We also found that OT administration selectively reduced functional coupling between the amygdala and areas in the occipital and inferior temporal cortex during the viewing of fearful and aggressive faces, but not during the viewing of neutral or appeasing faces. Taken together, our results indicate homologies between monkeys and humans in the neural circuits mediating the effects of OT. Thus, the monkey may be an ideal animal model to explore the development of OT-based pharmacological strategies for treating patients with dysfunctional social behavior.oxytocin | neuroimaging | nonhuman primate | social stimuli I n the last decade, oxytocin (OT), a mammalian hormone, has become one of the most studied peptides of the neuroendocrine system. In humans, accumulating evidence has demonstrated that OT affects a wide range of social behavior and cognition, including perception, recognition and memory of social stimuli (1-5), socially reinforced learning (6), and more complex sociocognitive behaviors [e.g., trust (7,8), cooperation (9), generosity (10), and empathy (6, but see ref. 11)]. Therefore, it has been proposed that OT may serve as a treatment for various disorders with dysfunctional social behavior, such as autism spectrum disorders, antisocial personality disorder, and schizophrenia (for review, see ref. 12). A recent study found that OT enhances brain activity for socially meaningful stimuli but attenuates activity for nonsocially meaningful stimuli in children with autism spectrum disorders (13). Although these studies suggest very promising prospects of OT for clinical use, the neural mechanisms underlying OT's modulatory effects remain elusive. To understand these mechanisms, it is important to investigate the effect of OT on brain activity, especially in regions involved in social behavior and cognition.Functional magnetic resonance imaging (fMRI) has been the major approach to investigating altered brain activation patterns in response to OT in humans. OT may affect the per...

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Section: Discussionmentioning

confidence: 99%

Oxytocin modulates fMRI responses to facial expression in macaques

Liu¹,

Hadj-Bouziane²,

Jones³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…However, key evidence argues against that explanation. First, a recent examination of FEF inputs to V4 found that a vast majority of the FEF input to V4 consists of excitatory synapses onto pyramidal neurons (Anderson et al, 2011). In addition, microstimulation of the FEF rapidly increases the magnitude and selectivity of V4 visual responses (Moore and Armstrong, 2003;Armstrong and Moore, 2007) suggesting that the direct projections from the FEF exert an excitatory, gain modulation on visually driven inputs to V4.…”

Section: Sources Of Presaccadic Enhancement In V4mentioning

confidence: 99%

“…It could be that inactivation of the FEF similarly results in compensatory effects within the SC, and this compensation influences presaccadic enhancement in V4 via a tectopulvinar-dorsal stream route, perhaps involving area LIP. Alternatively, there could be a compensatory increase in presaccadic activity within LIP itself, and this compensation could be conveyed directly to V4 (Andersen et al, 1990).…”

Section: Sources Of Presaccadic Enhancement In V4mentioning

confidence: 99%

“…FEF neurons show a mix of visual and motor response properties (Bruce and Goldberg, 1985), and their activity reflects the location of covert attention . FEF neurons are reciprocally connected with multiple extrastriate visual areas, including V4 (Stanton et al, 1995), where FEF projects predominantly excitatory inputs directly onto pyramidal neurons (Anderson et al, 2011). To test the contribution of the FEF to presaccadic modulation in visual cortex, we measured the effects of FEF inactivation on V4 activity during visually guided saccades.…”

Section: Introductionmentioning

confidence: 99%

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A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets

2014

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The responses of neurons within posterior visual cortex are enhanced when response field (RF) stimuli are targeted with saccadic eye movements. Although the motor-related activity within oculomotor structures seems a likely source of the enhancement, the origin of the modulation is unknown. We tested the role of the frontal eye field (FEF) in driving presaccadic modulation in area V4 by inactivating FEF neurons at retinotopically corresponding sites within the macaque monkey (Macaca mulatta) brain. As previously observed, FEF inactivation produced profound, and spatially specific, deficits in memory-guided saccades, and increased the latency, scatter, and duration of visually guided saccades. Despite the clear behavioral deficits, we found that rather than being eliminated or reduced by FEF inactivation, presaccadic enhancement of V4 activity was increased. FEF inactivation nonetheless diminished the stimulus discriminability of V4 visual responses both during fixation and in the presaccadic period. Thus, without input from the FEF, V4 neurons signaled more about the direction of saccades and less about the features of the saccadic target. In addition, FEF inactivation significantly increased the suppressive effects of non-RF stimuli on V4 activity. These results reveal multiple sources of presaccadic modulation in V4 and suggest that the FEF contributes uniquely to the presaccadic specification of visual target features.

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“…Anatomical studies have shown reciprocal connections between the FEF and LIP (Anderson et al 2011;Huerta et al 1987;Stanton et al 1995), and the areas share many neuronal characteristics. Furthermore, imaging studies have shown the activation of a frontoparietal network during attention tasks (Corbetta et al 1998;Nobre et al 2000;Wardak et al 2010), and FEF microstimulation causes enhanced functional magnetic resonance imaging (fMRI) activation in LIP, even in the absence of visual stimulation (Ekstrom et al 2008).…”

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confidence: 99%

Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Premereur

Vanduffel

Roelfsema

et al. 2012

Journal of Neurophysiology

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Premereur E, Vanduffel W, Roelfsema PR, Janssen P. Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area. J Neurophysiol 108: 1392-1402, 2012. First published June 6, 2012 doi:10.1152/jn.00323.2012.-Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time-and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for taskdependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.

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Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

Cited by 102 publications

References 60 publications

Oxytocin modulates fMRI responses to facial expression in macaques

Oxytocin modulates fMRI responses to facial expression in macaques

A Distinct Contribution of the Frontal Eye Field to the Visual Representation of Saccadic Targets

Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

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