scholarly journals Axonal plasticity associated with perceptual learning in adult macaque primary visual cortex

2018 ◽  
Vol 115 (41) ◽  
pp. 10464-10469 ◽  
Author(s):  
Timo van Kerkoerle ◽  
Sally A. Marik ◽  
Stephan Meyer zum Alten Borgloh ◽  
Charles D. Gilbert

Perceptual learning is associated with changes in the functional properties of neurons even in primary sensory areas. In macaque monkeys trained to perform a contour detection task, we have observed changes in contour-related facilitation of neuronal responses in primary visual cortex that track their improvement in performance on a contour detection task. We have previously explored the anatomical substrate of experience-dependent changes in the visual cortex based on a retinal lesion model, where we find sprouting and pruning of the axon collaterals in the cortical lesion projection zone. Here, we attempted to determine whether similar changes occur under normal visual experience, such as that associated with perceptual learning. We labeled the long-range horizontal connections in visual cortex by virally mediated transfer of genes expressing fluorescent probes, which enabled us to do longitudinal two-photon imaging of axonal arbors over the period during which animals improve in contour detection performance. We found that there are substantial changes in the axonal arbors of neurons in cortical regions representing the trained part of the visual field, with sprouting of new axon collaterals and pruning of preexisting axon collaterals. Our findings indicate that changes in the structure of axonal arbors are part of the circuit-level mechanism of perceptual learning, and further support the idea that the learned information is encoded at least in part in primary visual cortex.

2018 ◽  
Vol 115 (41) ◽  
pp. 10499-10504 ◽  
Author(s):  
Yin Yan ◽  
Li Zhaoping ◽  
Wu Li

Early sensory cortex is better known for representing sensory inputs but less for the effect of its responses on behavior. Here we explore the behavioral correlates of neuronal responses in primary visual cortex (V1) in a task to detect a uniquely oriented bar—the orientation singleton—in a background of uniformly oriented bars. This singleton is salient or inconspicuous when the orientation contrast between the singleton and background bars is sufficiently large or small, respectively. Using implanted microelectrodes, we measured V1 activities while monkeys were trained to quickly saccade to the singleton. A neuron’s responses to the singleton within its receptive field had an early and a late component, both increased with the orientation contrast. The early component started from the outset of neuronal responses; it remained unchanged before and after training on the singleton detection. The late component started ∼40 ms after the early one; it emerged and evolved with practicing the detection task. Training increased the behavioral accuracy and speed of singleton detection and increased the amount of information in the late response component about a singleton’s presence or absence. Furthermore, for a given singleton, faster detection performance was associated with higher V1 responses; training increased this behavioral–neural correlate in the early V1 responses but decreased it in the late V1 responses. Therefore, V1’s early responses are directly linked with behavior and represent the bottom-up saliency signals. Learning strengthens this link, likely serving as the basis for making the detection task more reflexive and less top-down driven.


1991 ◽  
Vol 305 (3) ◽  
pp. 370-392 ◽  
Author(s):  
Barbara A. McGuire ◽  
Charles D. Gilbert ◽  
Patricia K. Rivlin ◽  
Torsten N. Wiesel

Author(s):  
Jinwoo Kim ◽  
Min Song ◽  
Se-Bum Paik

AbstractIn the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye opening. Here, we show that LHCs in V1 may originate from spatio-temporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by co-activating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching topography of the underlying orientation map. We also confirmed that the model can also reproduce orientation-specific microcircuits in salt-and-pepper organizations in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits.HighlightsDevelopmental model of long-range horizontal connections (LHCs) in V1 is simulatedSpontaneous retinal waves generate feature-specific wiring of LHCs in visual cortexEmerged LHCs induce orientation-matching patterns of spontaneous cortical activityRetinal waves induce orientation-specific microcircuits of visual cortex in rodentsSignificance statementLong-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, selectively connecting iso-domains of orientation maps. However, it is unknown how such tuning-specific wirings develop before eye-opening. Here, we show that LHCs in V1 originate from the tuning-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings of V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is applicable universally to circuits of various mammalian species.


Neuron ◽  
2008 ◽  
Vol 57 (6) ◽  
pp. 799-801 ◽  
Author(s):  
David Carmel ◽  
Marisa Carrasco

1997 ◽  
Vol 14 (2) ◽  
pp. 241-251 ◽  
Author(s):  
Anne K. Wiser ◽  
Edward M. Callaway

AbstractTo study the relationship between ocular dominance columns (ODCs) and axonal projections of individual layer 6 pyramidal neurons in the primary visual cortex, neurons were intracellularly labeled with biocytin in live slices prepared from macaque monkeys that had received an intravitreal injection of tetrodotoxin (TTX). The TTX injection indirectly causes a decrease in cytochrome oxidase (CO) expression in the cortical ODCs corresponding to the treated eye (Wong-Riley & Carroll, 1984). Sections from slices with labeled layer 6 neurons were double stained for biocytin and CO, to allow visualization of neuronal processes as well as ODCs. Twenty-seven layer 6 pyramidal neurons in ODC-labeled slices were analyzed. These neurons were classified according to the criteria of Wiser and Callaway (1996). Eight of these are class I neurons, which have dense axonal projections to the monocular layer 4C. The remaining 19 are class II neurons which project primarily to the binocular layers outside 4C. Among class I neurons, two have dense axonal arbors in layer 4Cα (type Iα), one in layer 4Cβ (type Iβ), and two throughout the depth of layer 4C (type IC). None of these neurons have ODC-specific axonal arbors. The remaining three class I neurons have focused axonal projections in layers 4Cβ and 4A (type IβA). All three appear to have axonal arbors predominantly within their home ODC in layer 4C. The axonal arbors of class II neurons do not appear to relate to ODCs in any specific fashion.


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