Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey

Heinen, Stephen; Skavenski, Alexander A.

doi:10.1007/bf00229845

Cited by 195 publications

(141 citation statements)

References 21 publications

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“…These findings pose a significant problem for fMRI and electrophysiological studies of cortical responses to scotomas reporting ectopic responses from a population of neurons in the SPZ as evidence of reorganization without taking into account effects of short-term adaptation (28)(29)(30)(31)(32)(33). Here, we achieved the same results in the SPZ of the rod scotoma with short-term exposure to scotopic conditions.…”

Section: Voxels With Prfs Overlapping the Rod Scotoma Show An Ectopicsupporting

confidence: 60%

“…Each of these measurements was independent of long-term plasticity, which has particularly important implications for the interpretation of studies of cortical reorganization. Although several electrophysiological and fMRI studies propose long-term cortical reorganization as the primary mechanism for silencing, ectopic shifts, and pRF scaling within the SPZ (29,(31)(32)(33)35), we have acquired a similar pRF-level measurement and shown that these responses can arise during short-term cortical adaptation in the representation of pRFs with some overlap with the SPZ.…”

Section: Discussionmentioning

confidence: 78%

“…Some groups using electrophysiology have reported silencing, ectopic shifts, and pRF scaling from V1 neurons within the SPZ that they use as evidence of cortical reorganization weeks to months after the retinae were lesioned (28)(29)(30)(31)(32)(33). However, because these studies typically measure only immediate postlesion and long-term (weeks to months) time points, they cannot differentiate responses in the SPZ caused by short-term adaptation from those arising from longterm reorganization (Fig.…”

Section: Comparisons With Studies On the Cortical Effects Of Other Rementioning

confidence: 99%

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fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

Barton

Brewer

2015

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

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Are silencing, ectopic shifts, and receptive field (RF) scaling in cortical scotoma projection zones (SPZs) the result of long-term reorganization (plasticity) or short-term adaptation? Electrophysiological studies of SPZs after retinal lesions in animal models remain controversial, because they are unable to conclusively answer this question because of limitations of the methodology. Here, we used functional MRI (fMRI) visual field mapping through population RF (pRF) modeling with moving bar stimuli under photopic and scotopic conditions to measure the effects of the rod scotoma in human early visual cortex. As a naturally occurring central scotoma, it has a large cortical representation, is free of traumatic lesion complications, is completely reversible, and has not reorganized under normal conditions (but can as seen in rod monochromats). We found that the pRFs overlapping the SPZ in V1, V2, V3, hV4, and VO-1 generally (i) reduced their blood oxygen level-dependent signal coherence and (ii) shifted their pRFs more eccentric but (iii) scaled their pRF sizes in variable ways. Thus, silencing, ectopic shifts, and pRF scaling in SPZs are not unique identifiers of cortical reorganization; rather, they can be the expected result of short-term adaptation. However, are there differences between rod and cone signals in V1, V2, V3, hV4, and VO-1? We did not find differences for all five maps in more peripheral eccentricities outside of rod scotoma influence in coherence, eccentricity representation, or pRF size. Thus, rod and cone signals seem to be processed similarly in cortex. can adult human visual cortex reorganize after the removal of visual input?" This question can be studied through the effects of retinal lesions (causing scotomas), in which input from the retina has been removed, but cortical representations of the scotoma projection zone (SPZ) remain intact. Accordingly, emphasis must be placed on teasing apart effects of scotomas that relate to short-term cortical adaptation from those of long-term cortical plasticity (1) (terminology review is in ref.2). Here, we investigate this question in human cortex by using functional MRI (fMRI) to measure the immediate cortical SPZ responses in the unique paradigm of the naturally occurring rod scotoma.The photoreceptors in humans can be divided into two classes: cones, which are primarily responsible for vision under high-luminance (photopic) conditions, and rods, which are primarily responsible for vision under low-luminance (scotopic) conditions when the cones are inactive. The cones are an order of magnitude more highly concentrated in the fovea relative to the periphery, where they inform our most detailed visual experience (3). In contrast, the greatest concentrations of rods are more than ∼10°e ccentric from fixation and become increasingly sparse toward fixation until they are completely absent. This roughly circular rodfree zone covers a radius of ∼0.6-0.8°of visual angle about the fixation point (diameter = ∼1.25-1.7°) (4, 5). Under scotopic conditions, a...

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Section: Voxels With Prfs Overlapping the Rod Scotoma Show An Ectopicsupporting

confidence: 60%

Section: Discussionmentioning

confidence: 78%

Section: Comparisons With Studies On the Cortical Effects Of Other Rementioning

confidence: 99%

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fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

Barton

Brewer

2015

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

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“…Does MT retinotopically reorganize to represent more of the preserved inputs from V1? Neurons in primary visual cortex acquire new receptive fields after being deprived by retinal lesions Heinen and Skavenski, 1991;Gilbert and Wiesel, 1992) (for review, see Kaas et al, 2001). Similar reorganizations might be expected in MT, because individual axons of neurons in V1 branch and form multiple terminal arbors over considerable distances in MT (Rockland, 1989).…”

Section: Discussionmentioning

confidence: 88%

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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“…Long-term changes were observed in primary auditory cortex as a result of cochlear lesions (Rajan, Irvine, Wise & Heil, 1993), and immediate changes were demonstrated in the same area as a result of learning (Weinberger, Hopkins & Diamond, 1984 (Eysel, GonzalezAguilar & Mayer, 1980;Eysel, Gonzalez-Aguilar & Mayer, 1981). Considering this demonstration in the LGN and the changes observed in somatosensory and auditory cortices, it is not surprising that the adult visual cortex can also reorganize (Kaas, Krubitzer, Chino, Langston, Polley & Blair, 1990;Heinen & Skavenski, 1991;Gilbert & Wiesel, 1992;Schmid, Rosa & Calford, 1993). However, the changes in primary visual cortex (V1) are not simply a reflection of those occurring in the LGN, since extensive changes in receptive field position can be observed a few hours after retinal laser lesions (Gilbert & Wiesel, 1992;Schmid, Calford & Rosa, 1994).…”

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confidence: 98%

Responsiveness of cat area 17 after monocular inactivation: limitation of topographic plasticity in adult cortex.

Rosa

Schmid

Calford

1995

The Journal of Physiology

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1. Recordings were made from neurones in the splenial sulcus of normal adult cats and adult cats which had one eye inactivated by enucleation or photocoagulation of the optic disc. Two visually responsive regions were observed, corresponding to the peripheral representation of visual area 1 (V1) and the splenial visual area. In normal animals, responses to the ipsilateral eye in Vl were restricted to the medial half of the splenial sulcus, up to 45-50 deg eccentricity. Thus, by inactivating the eye contralateral to the experimental hemisphere, we created a region in VI, 1-2 mm wide, that lacked normal inputs. 2. In contrast to results from previous experiments where lesions were placed in the central retina, neurones in the deprived peripheral representation remained unresponsive to light stimuli for up to 12 h after deactivation of the contralateral eye. 3. In animals that were allowed to recover from the monocular deactivation for periods of 2 days to 16 months, there was rearrangement of the retinotopic maps. Receptive fields in regions of cortex that normally represented the monocular crescent were displaced to the temporal border of the binocular field of vision. However, most neurones in the deprived peripheral representation remained unresponsive to visual stimuli even more than 1 year after treatment. This is also in marked contrast with the extensive reorganization that is observed in the central representation of Vi after restricted retinal lesions. Analysis of the cortical magnification factor demonstrates that the change in visual topography is local, and does not involve an overall centro-peripheral shift of the retinotopic map. 4. Among the neurones that did show displaced receptive fields, the response properties were clearly abnormal. They showed a notable lack of spontaneous activity, low firing rates and rapid habituation to repeated stimulation. 5. The low potential for reorganization of the monocular sector of Vl demonstrates that the capacity for plasticity of mature sensory representations varies with location in cortex. Even relatively small pieces of cortex, such as the monocular crescent representations, may not reorganize completely if certain conditions are not met. These results suggest the existence of natural boundaries that may limit the process of reorganization of sensory representations.The topographical maps that exist in adult sensory cortex have a considerable plastic capacity. This was first observed in the somatosensory cortex, where immediate and chronic changes of receptive field size and location were described following amputation (e

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Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey

Cited by 195 publications

References 21 publications

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

fMRI of the rod scotoma elucidates cortical rod pathways and implications for lesion measurements

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

Responsiveness of cat area 17 after monocular inactivation: limitation of topographic plasticity in adult cortex.

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