Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal

Rodman, Hillary R.; Gross, Charles G.; Albright, Thomas D.

doi:10.1523/jneurosci.09-06-02033.1989

Cited by 309 publications

(250 citation statements)

References 54 publications

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“…We found that neurons within the lesion projection zones of MT are strongly direction-selective, similar to those in normal marmoset MT. This result is in agreement with previous work in the macaque (Rodman et al, 1989;Girard et al, 1992). The fact that even neurons with displaced receptive fields show strong direction selectivity argues against the notion that this property is simply imposed on MT cells by afferents from hierarchically "lower" areas.…”

Section: Discussionsupporting

confidence: 92%

“…Lesions (Rodman et al, 1989) or brief inactivations (Bullier et al, 1994) of V1 in Old World monkeys do not completely abolish the visual responses of cells in some extrastriate areas, including the middle temporal area (MT), a result that is compatible with the above hypothesis. In contrast, a study in New World monkeys (Aotus trivirgatus) in which MT was studied immediately after a V1 lesion reported no residual activity in the sector of MT that corresponded, in visuotopic coordinates, to the destroyed part of V1 (Krubitzer and Kaas, 1992).…”

Section: Abstract: Marmoset; Vision; Extrastriate; Receptive Fields;mentioning

confidence: 54%

“…Using a lesion paradigm similar to the one adopted here, Rodman et al (1989) demonstrated that a significant proportion of MT cells in the macaque remain responsive and retain direction selectivity after V1 lesions. Our results in the marmoset, a New World monkey with diurnal habits, support this claim.…”

Section: Discussionmentioning

confidence: 89%

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Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

2000

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In primates, lesions of striate cortex (V1) result in scotomas in which only rudimentary visual abilities remain. These aspects of vision that survive V1 lesions have been attributed to direct thalamic pathways to extrastriate areas, including the middle temporal area (MT). However, studies in New World monkeys and humans have questioned this interpretation, suggesting that remnants of V1 are responsible for both the activation of MT and residual vision. We studied the visual responses of neurons in area MT in New World marmoset monkeys in the weeks after lesions of V1. The extent of the scotoma in each case was estimated by mapping the receptive fields of cells located near the lesion border and by histological reconstruction. Two response types were observed among the cells located in the part of MT that corresponds, in visuotopic coordinates, to the lesioned part of V1. Many neurons (62%) had receptive fields that were displaced relative to their expected location, so that they represented the visual field immediately surrounding the scotoma. This may be a consequence of a process analogous to the reorganization of the V1 map after retinal lesions. However, another 20% of the cells had receptive fields centered inside the scotoma. Most of these neurons were strongly directionselective, similar to normal MT cells. These results show that MT cells differ in their responses to lesioning of V1 and that only a subpopulation of MT neurons can be reasonably linked to residual vision and blindsight.

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Section: Discussionsupporting

confidence: 92%

Section: Abstract: Marmoset; Vision; Extrastriate; Receptive Fields;mentioning

confidence: 54%

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Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

2000

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“…The same rank order applies to these stations in terms of processing because neuronal selectivity for orientation and the direction of movement is not present in the lateral geniculate but emerges for the first time in the primary visual cortex. Similarly, neuronal selectivity for stimulus velocity emerges in the middle temporal (MT) area which is anatomically at least two levels away from the primary visual cortex Maunsell and Newsome 1987;De Yoe and Van Essen, 1988;Livingstone and Hubel 1988), although the contributions of inputs other than the striate cortex and V2 to the stimulus selectivities of MT neurons make a simple serial hierarchy unlikely (Rodman et al 1989). …”

Section: Convergence Of Parallel Pathwaysmentioning

confidence: 99%

Similar Algorithms in Different Sensory Systems and Animals

Konishi

1990

Cold Spring Harbor Symposia on Quantitative Biology

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Animals must both recognize and localize the sensory signals essential for their survival and reproduction. Certain cues contained in a signal define its identity and location. Such cues include, for example, the temporal pattern of song for species recognition in crickets and binaural disparities for sound localization in owls. One can predict potential cues and the methods of using them from consideration of the physical attributes of the signal for the task. The discovery of the real cue that is used by the animal. however, requires study of the animal's response to different potential cues.Once the real cue is identified, the next question is how is it encoded in the language of the nervous system? One can develop an algorithm for the solution of the coding problem. There are, however, many possible ways of solving the same problem. There is, however, no theoretical means of identifying the real algorithm. Analysis of neuronal responses to stimuli and study of the connections between neurons may inform us about the coding scheme because the connections and signals between neurons underlie the coding mechanisms, but what neurons tell depends on what question the investigator asks. As Barlow ( 1972) pointed out, " ... neurophysiology and sensation are best linked by looking at the flow of information rather than simpler measures of neuronal activity .. , A neurophysiological investigation of how information is transformed from lower-to higher-order stations may be difficult because information processing is highly nonlinear. Going in the opposite direction. the "topdown" approach is easier in some systems because one starts with the knowledge of what is encoded at the top or at a relatively higher station. The criterion for encoding is the stimulus selectivity of single neurons. The flow of information is therefore inferred from the stimulus selectivities recorded in interconnected stations. For example, the neurons of the external nucleus of the inferior colliculus in the barn owl respond selectively to a combination of interaural time and intensity differences. The neuronal selectivities for these binaural cues have been traced from this nucleus back to the first sites where the selectivities emerge and the pathways for the flow of information can be established .The approach that looks for the flow of information has been used only in a few complex neural systems including the visual system of the macaque monkey (for review, see Van Essen

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“…Girard et al (1991b) found that some neurons in V3a (dorsomedial area, DM) continued to respond to visual stimuli after the relevant portion of V1 was inactivated by cooling, and Rodman et al (1989) found that some neurons in MT retained responsiveness after lesions of V1 (for related results, see Girard et al, 1992). Because neurons in MT failed to respond to visual stimuli in monkeys with both V1 and superior colliculus (SC) lesions, a relay of visual information from the SC to the pulvinar and then to extrastriate cortex was postulated as the source of the visual activation of MT in the absence of V1 (Rodman et al, 1990).…”

Section: Introductionmentioning

confidence: 99%

Responses of Neurons in the Middle Temporal Visual Area After Long-Standing Lesions of the Primary Visual Cortex in Adult New World Monkeys

2003

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The retinotopic organization of the middle temporal visual area (MT) was determined in six adult owl monkeys and one adult marmoset 69 d to 10 months after lesions of the dorsolateral primary visual cortex (V1). The lesions removed were limited to extensive parts of the representation of the lower visual quadrant in V1. Microelectrodes were used to record from neurons at numerous sites in MT to determine whether parts of MT normally devoted to the lower visual quadrant (1) were unresponsive to visual stimuli, (2) acquired responsiveness to inputs from intact portions of V1, or (3) became responsive to some other visually driven input such as a relay from the superior colliculus via the pulvinar to MT. All monkeys (n ϭ 6) with moderate to moderately large lesions had unresponsive portions of MT even after 10 months of recovery. These unresponsive regions were retinotopically equivalent to the removed parts of V1 in normal animals. Thus, there was no evidence for an alternative source of activation. In addition, these results indicate that any retinotopic reorganization of MT based on inputs from intact portions of V1 was not extensive, yet neurons near the margins of responsive cortex may have acquired new receptive fields, and the smallest 5°lesion of V1 failed to produce an unresponsive zone. Deprived portions of MT were not remarkably changed in histological appearance in cytochrome oxidase, Nissl, and Wisteria floribunda agglutinin preparations. Nevertheless, some reduction in myelin staining and other histological changes were suggested. We conclude that MT is highly dependent on V1 for activation in these monkeys, and alternative sources do not become effective over months when normal activation is absent. Additionally, remaining V1 inputs have only a limited capacity to expand their activation territory into deprived portions of MT.

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Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal

Cited by 309 publications

References 54 publications

Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex

Similar Algorithms in Different Sensory Systems and Animals

Responses of Neurons in the Middle Temporal Visual Area After Long-Standing Lesions of the Primary Visual Cortex in Adult New World Monkeys

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