Spatial Modulation of Primate Inferotemporal Responses by Eye Position

Lehky, Sidney R.; Peng, Xinmiao; McAdams, Carrie J.; Sereno, Anne B.

doi:10.1371/journal.pone.0003492

Cited by 28 publications

(36 citation statements)

References 69 publications

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“…On the other hand, the position-selectivity in CDt neurons is unexpected, since position selectivity tends to become weaker along the ventral visual pathway (Boussaoud et al, 1991). One explanation would be that object-selective neurons in the inferotemporal cortex (ITC) may carry position information (Op De Beeck and Vogels, 2000; DiCarlo and Maunsell, 2003; Lehky et al, 2008; Sereno and Lehky, 2011). In addition to receiving inputs from the anterior ITC, individual CDt neurons may receive inputs from multiple cortical areas along the ventral visual pathway, including the areas in its earlier stages, such as the central and posterior ITCs, and area V4, which retain some positional information.…”

Section: Discussionmentioning

confidence: 99%

What and Where Information in the Caudate Tail Guides Saccades to Visual Objects

et al. 2012

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We understand the world by making saccadic eye movements to various objects. However, it is unclear how a saccade can be aimed at a particular object, because two kinds of visual information, what the object is and where it is, are processed separately in the dorsal and ventral visual cortical pathways. Here we provide evidence suggesting that a basal ganglia circuit through the tail of the monkey caudate nucleus (CDt) guides such object-directed saccades. First, many CDt neurons responded to visual objects depending on where and what the objects were. Second, electrical stimulation in the CDt induced saccades whose directions matched the preferred directions of neurons at the stimulation site. Third, many CDt neurons increased their activity before saccades directed to the neurons’ preferred objects and directions in a free-viewing condition. Our results suggest that CDt neurons receive both ‘what’ and ‘where’ information and guide saccades to visual objects.

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Section: Discussionmentioning

confidence: 99%

What and Where Information in the Caudate Tail Guides Saccades to Visual Objects

et al. 2012

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“…It is well-known that areas V3v, V4 have retinotopy, but, more surprisingly, sensitivity to retinotopic information is observed in neurons of macaque area IT (Lueschow et al, 1994; Op De Beeck and Vogels, 2000; DiCarlo and Maunsell, 2003). Lehky et al (2008) states, “With respect to retinal position, about two-thirds of AIT neurons were sensitive to modest shifts in the retinal stimulus location. While from one perspective this retinotopic modulation is simply a manifestation of the existence of a receptive field, from another perspective it indicates that inferotemporal cortex retains information about the spatial position of objects in retinocentric coordinates.” Lehky and Sereno (2011) built on these findings in a model that had IT neurons with realistically large receptive fields, nonetheless had exquisite position selectivity and localization.…”

Section: Our Proposal: Exploration and Exploitationmentioning

confidence: 99%

Two Visual Pathways in Primates Based on Sampling of Space: Exploitation and Exploration of Visual Information

Sheth

Young

2016

Front. Integr. Neurosci.

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Evidence is strong that the visual pathway is segregated into two distinct streams—ventral and dorsal. Two proposals theorize that the pathways are segregated in function: The ventral stream processes information about object identity, whereas the dorsal stream, according to one model, processes information about either object location, and according to another, is responsible in executing movements under visual control. The models are influential; however recent experimental evidence challenges them, e.g., the ventral stream is not solely responsible for object recognition; conversely, its function is not strictly limited to object vision; the dorsal stream is not responsible by itself for spatial vision or visuomotor control; conversely, its function extends beyond vision or visuomotor control. In their place, we suggest a robust dichotomy consisting of a ventral stream selectively sampling high-resolution/focal spaces, and a dorsal stream sampling nearly all of space with reduced foveal bias. The proposal hews closely to the theme of embodied cognition: Function arises as a consequence of an extant sensory underpinning. A continuous, not sharp, segregation based on function emerges, and carries with it an undercurrent of an exploitation-exploration dichotomy. Under this interpretation, cells of the ventral stream, which individually have more punctate receptive fields that generally include the fovea or parafovea, provide detailed information about object shapes and features and lead to the systematic exploitation of said information; cells of the dorsal stream, which individually have large receptive fields, contribute to visuospatial perception, provide information about the presence/absence of salient objects and their locations for novel exploration and subsequent exploitation by the ventral stream or, under certain conditions, the dorsal stream. We leverage the dichotomy to unify neuropsychological cases under a common umbrella, account for the increased prevalence of multisensory integration in the dorsal stream under a Bayesian framework, predict conditions under which object recognition utilizes the ventral or dorsal stream, and explain why cells of the dorsal stream drive sensorimotor control and motion processing and have poorer feature selectivity. Finally, the model speculates on a dynamic interaction between the two streams that underscores a unified, seamless perception. Existing theories are subsumed under our proposal.

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“…More recently, eye position has also been demonstrated to modulate neural responses in the ventral visual stream, including cells in V4 (Bremmer, 2000; Rosenbluth and Allman, 2002), inferotemporal cortex (Lehky et al, 2008), as well as hippocampus and parahippocampus (Ringo et al, 1994). …”

Section: Introductionmentioning

confidence: 99%

Recovering stimulus locations using populations of eye-position modulated neurons in dorsal and ventral visual streams of non-human primates

Sereno¹,

Sereno²,

Lehky³

2014

Front. Integr. Neurosci.

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We recorded visual responses while monkeys fixated the same target at different gaze angles, both dorsally (lateral intraparietal cortex, LIP) and ventrally (anterior inferotemporal cortex, AIT). While eye-position modulations occurred in both areas, they were both more frequent and stronger in LIP neurons. We used an intrinsic population decoding technique, multidimensional scaling (MDS), to recover eye positions, equivalent to recovering fixated target locations. We report that eye-position based visual space in LIP was more accurate (i.e., metric). Nevertheless, the AIT spatial representation remained largely topologically correct, perhaps indicative of a categorical spatial representation (i.e., a qualitative description such as “left of” or “above” as opposed to a quantitative, metrically precise description). Additionally, we developed a simple neural model of eye position signals and illustrate that differences in single cell characteristics can influence the ability to recover target position in a population of cells. We demonstrate for the first time that the ventral stream contains sufficient information for constructing an eye-position based spatial representation. Furthermore we demonstrate, in dorsal and ventral streams as well as modeling, that target locations can be extracted directly from eye position signals in cortical visual responses without computing coordinate transforms of visual space.

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Spatial Modulation of Primate Inferotemporal Responses by Eye Position

Cited by 28 publications

References 69 publications

What and Where Information in the Caudate Tail Guides Saccades to Visual Objects

What and Where Information in the Caudate Tail Guides Saccades to Visual Objects

Two Visual Pathways in Primates Based on Sampling of Space: Exploitation and Exploration of Visual Information

Recovering stimulus locations using populations of eye-position modulated neurons in dorsal and ventral visual streams of non-human primates

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