TrkB Activation during a Critical Period Mimics the Protective Effects of Early Visual Experience on Perception and the Stability of Receptive Fields in Adult Superior Colliculus

Sensory deprivation is thought to have an adverse effect on visual development and to prolong the critical period for plasticity. Once the animal reaches adulthood, however, synaptic connectivity is understood to be largely stable. We reported previously that N-methyl-d-aspartate (NMDA) receptor blockade in the superior colliculus of the Syrian hamster prevents refinement of receptive fields (RFs) in normal or compressed retinotopic projections, resulting in target neurons with enlarged RFs but normal stimulus tuning. Here we asked whether visually driven activity is necessary for refinement or maintenance of retinotopic maps or if spontaneous activity is sufficient. Animals were deprived of light either in adulthood only or from birth until the time of recording. We found that dark rearing from birth to 2 mo of age had no effect on the timing and extent of RF refinement as assessed with single unit extracellular recordings. Visual deprivation in adulthood also had no effect. Continuous dark rearing from birth into adulthood, however, resulted in a progressive loss of refinement, resulting in enlarged, asymmetric receptive fields and altered surround suppression in adulthood. Thus unlike in visual cortex, early visually driven activity is not necessary for refinement of receptive fields during development, but is required to maintain refined visual projections in adulthood. Because the map can refine normally in the dark, these results argue against a deprivation-induced delay in critical period closure, and suggest instead that early visual deprivation leaves target neurons more vulnerable to deprivation that continues after refinement.

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TrkB Activation During a Critical Period Mimics the Protective Effects of Early Visual Experience on Perception and the Stability of Receptive Fields in Adult Superior Colliculus

10.1101/435784 ◽

2018 ◽

Author(s):

David B. Mudd ◽

Timothy S. Balmer ◽

So Yeon Kim ◽

Noura Machhour ◽

Sarah L. Pallas

Keyword(s):

Visual Acuity ◽

Visual Cortex ◽

Receptive Field ◽

Superior Colliculus ◽

Spontaneous Activity ◽

Signaling Pathway ◽

Critical Period ◽

Visual Experience ◽

Receptive Fields ◽

Trkb Receptors

AbstractDuring a critical period in development, spontaneous and evoked retinal activity shape visual pathways in an adaptive fashion. Interestingly, spontaneous activity is sufficient for spatial refinement of visual receptive fields in superior colliculus (SC) and visual cortex (V1), but early visual experience is necessary to maintain inhibitory synapses and stabilize RFs in adulthood (Carrasco et al. 2005, 2011; Carrasco & Pallas 2006; Balmer & Pallas 2015a). In visual cortex (V1), brain-derived neurotrophic factor (BDNF) and its high affinity receptor TrkB are important for development of visual acuity, inhibition, and regulation of the critical period for ocular dominance plasticity (Hanover et al., 1999; Huang et al., 1999; Gianfranceschi et al., 2003). To examine the generality of this signaling pathway for visual system plasticity, the present study examined the role of TrkB signaling during the critical period for RF refinement in SC. Activating TrkB receptors during the critical period (P33-40) in DR subjects produced normally refined RFs, and blocking TrkB receptors in light-exposed animals resulted in enlarged adult RFs like those in DR animals. We also report here that deprivation- or TrkB blockade-induced RF enlargement in adulthood impaired fear responses to looming overhead stimuli, and negatively impacted visual acuity. Thus, early TrkB activation is both necessary and sufficient to maintain visual RF refinement, robust looming responses, and visual acuity in adulthood. These findings suggest a common signaling pathway exists for the maturation of inhibition between V1 and SC.Significance StatementReceptive field refinement in superior colliculus (SC) differs from more commonly studied examples of critical period plasticity in visual pathways in that it does not require visual experience to occur; rather spontaneous activity is sufficient. Maintenance of refinement beyond puberty requires a brief, early exposure to light in order to stabilize the lateral inhibition that shapes receptive fields. We find that TrkB activation during a critical period can substitute for visual experience in maintaining receptive field refinement into adulthood, and that this maintenance is beneficial to visual survival behaviors. Thus, as in some other types of plasticity, TrkB signaling plays a crucial role in RF refinement.

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Beyond the labeled line: variation in visual reference frames from intraparietal cortex to frontal eye fields and the superior colliculus

10.1101/124628 ◽

2017 ◽

Author(s):

V. C. Caruso ◽

D. S. Pages ◽

M. A. Sommer ◽

J. M. Groh

Keyword(s):

Receptive Field ◽

Superior Colliculus ◽

Reference Frames ◽

Receptive Fields ◽

Visual Signals ◽

Eye Position ◽

Frontal Eye Fields ◽

Response Patterns ◽

The Stability ◽

Retinal Information

ABSTRACTWe accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. We assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single unit activity was assessed in head-restrained monkeys performing visually-guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of hybrid representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read-out.New & NoteworthyHow we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labelled-line code for stimuli across saccades.

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Beyond the labeled line: variation in visual reference frames from intraparietal cortex to frontal eye fields and the superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.00584.2017 ◽

2018 ◽

Vol 119 (4) ◽

pp. 1411-1421 ◽

Cited By ~ 9

Author(s):

Valeria C. Caruso ◽

Daniel S. Pages ◽

Marc A. Sommer ◽

Jennifer M. Groh

Keyword(s):

Receptive Field ◽

Superior Colliculus ◽

Reference Frames ◽

Receptive Fields ◽

Visual Signals ◽

Eye Position ◽

Frontal Eye Fields ◽

Response Patterns ◽

The Stability ◽

Retinal Information

We accurately perceive the visual scene despite moving our eyes ~3 times per second, an ability that requires incorporation of eye position and retinal information. In this study, we assessed how this neural computation unfolds across three interconnected structures: frontal eye fields (FEF), intraparietal cortex (LIP/MIP), and the superior colliculus (SC). Single-unit activity was assessed in head-restrained monkeys performing visually guided saccades from different initial fixations. As previously shown, the receptive fields of most LIP/MIP neurons shifted to novel positions on the retina for each eye position, and these locations were not clearly related to each other in either eye- or head-centered coordinates (defined as hybrid coordinates). In contrast, the receptive fields of most SC neurons were stable in eye-centered coordinates. In FEF, visual signals were intermediate between those patterns: around 60% were eye-centered, whereas the remainder showed changes in receptive field location, boundaries, or responsiveness that rendered the response patterns hybrid or occasionally head-centered. These results suggest that FEF may act as a transitional step in an evolution of coordinates between LIP/MIP and SC. The persistence across cortical areas of mixed representations that do not provide unequivocal location labels in a consistent reference frame has implications for how these representations must be read out. NEW & NOTEWORTHY How we perceive the world as stable using mobile retinas is poorly understood. We compared the stability of visual receptive fields across different fixation positions in three visuomotor regions. Irregular changes in receptive field position were ubiquitous in intraparietal cortex, evident but less common in the frontal eye fields, and negligible in the superior colliculus (SC), where receptive fields shifted reliably across fixations. Only the SC provides a stable labeled-line code for stimuli across saccades.

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Early visual experience prevents but cannot reverse deprivation-induced loss of refinement in adult superior colliculus

Visual Neuroscience ◽

10.1017/s0952523806230177 ◽

2006 ◽

Vol 23 (6) ◽

pp. 845-852 ◽

Cited By ~ 10

Author(s):

MARÍA MAGDALENA CARRASCO ◽

SARAH L. PALLAS

Keyword(s):

Visual System ◽

Superior Colliculus ◽

Visual Experience ◽

Time Window ◽

Brain Plasticity ◽

Light Exposure ◽

Receptive Fields ◽

Adult Brain ◽

Early Postnatal Development ◽

Dark Rearing

The role of sensory experience in the development and plasticity of the visual system has been widely studied. It has generally been reported that once animals reach adulthood, experience-dependent visual plasticity is reduced. We have found that visual experience is not needed for the refinement of receptive fields (RFs) in the superior colliculus (SC) but instead is necessary to maintain them in adulthood (Carrasco et al., 2005). Without light exposure, RFs in SC of hamsters refine by postnatal day 60 as usual but then enlarge, presumably reducing visual acuity. In this study we examine whether a brief period of light exposure during early postnatal development would be sufficient to prevent RF enlargement in adulthood, and whether prolonged light exposure in adulthood could reverse the deprivation-induced increase in RF size. We found that an early postnatal period of at least 30 days of visual experience was sufficient to maintain refined RFs in the adult SC. Prolonged visual experience in adulthood could not reverse the RF enlargement resulting from long-term dark rearing, reflecting a loss of plasticity at this age. Our results suggest that, unlike in visual cortex, dark rearing does not indefinitely extend the critical period of plasticity in SC. Rather, there is a limited time window when early experience can protect RFs from the detrimental effects of visual deprivation in adulthood. These results contribute to understanding adult brain plasticity and argue for the importance of early visual experience in protecting the adult visual system.

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Ultrastructure of developing visual cortical synapses in the cat superior colliculus

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100085083 ◽

1991 ◽

Vol 49 ◽

pp. 156-157

Author(s):

Caroline A. Miller ◽

Laura L. Bruce

Keyword(s):

Superior Colliculus ◽

Phosphate Buffer ◽

Receptive Fields ◽

Visual Cortical Area ◽

Cortical Synapses ◽

Visual Cortical ◽

And Function ◽

Phosphate Buffered Saline ◽

The Brain ◽

Cat Superior Colliculus

The first visual cortical axons arrive in the cat superior colliculus by the time of birth. Adultlike receptive fields develop slowly over several weeks following birth. The developing cortical axons go through a sequence of changes before acquiring their adultlike morphology and function. To determine how these axons interact with neurons in the colliculus, cortico-collicular axons were labeled with biocytin (an anterograde neuronal tracer) and studied with electron microscopy.Deeply anesthetized animals received 200-500 nl injections of biocytin (Sigma; 5% in phosphate buffer) in the lateral suprasylvian visual cortical area. After a 24 hr survival time, the animals were deeply anesthetized and perfused with 0.9% phosphate buffered saline followed by fixation with a solution of 1.25% glutaraldehyde and 1.0% paraformaldehyde in 0.1M phosphate buffer. The brain was sectioned transversely on a vibratome at 50 μm. The tissue was processed immediately to visualize the biocytin.

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Auditory response properties of neurons in deep layers of cat superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1983.49.3.674 ◽

1983 ◽

Vol 49 (3) ◽

pp. 674-685 ◽

Cited By ~ 70

Author(s):

L. Z. Wise ◽

D. R. Irvine

Keyword(s):

Superior Colliculus ◽

Free Field ◽

Receptive Fields ◽

Great Majority ◽

Noise Burst ◽

Preliminary Evidence ◽

Excitatory Input ◽

Response Properties ◽

Deep Layers ◽

Spatial Fields

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.

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Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats

Journal of Neurophysiology ◽

10.1152/jn.1976.39.3.613 ◽

1976 ◽

Vol 39 (3) ◽

pp. 613-630 ◽

Cited By ~ 53

Author(s):

W. Singer ◽

F. Tretter

Keyword(s):

Electrical Stimulation ◽

Receptive Field ◽

Visual Experience ◽

Receptive Fields ◽

Direction Selectivity ◽

Connectivity Pattern ◽

Area 18 ◽

Efferent Connections ◽

Receptive Field Properties ◽

Areas 17 And 18

An attempt was made to relate the alterations of cortical receptive fields as they result from binocular visual deprivation to changes in afferent, intrinsic, and efferent connections of the striate and parastriate cortex. The experiments were performed in cats aged at least 1 jr with their eyelids sutured closed from birth.The results of the receptive-field analysis in A17 confirmed the reduction of light-responsive cells, the occasional incongruity of receptive-field properties in the two eyes, and to some extent also the loss of orientation and direction selectivity as reported previously. Other properties common to numerous deprived receptive fields were the lack of sharp inhibitory sidebands and the sometimes exceedingly large size of the receptive fields. Qualitatively as well as quantitatively, similar alterations were observed in area 18. A rather high percentage of cells in both areas had, however, preserved at least some orientation preference, and a few receptive fields had tuning properties comparable to those in normal cats. The ability of area 18 cells in normal cats to respond to much higher stimulus velocities than area 17 cells was not influenced by deprivation.The results obtained with electrical stimulation suggest two main deprivation effects: 1) A marked decrease in the safety factor of retinothalamic and thalamocortical transmission. 2) A clear decrease in efficiency of intracortical inhibition. But the electrical stimulation data also show that none of the basic principles of afferent, intrinsic, and efferent connectivity is lost or changed by deprivation. The conduction velocities in the subcortical afferents and the differentiation of the afferents to areas 17 and 18 into slow- and fast-conducting projection systems remain unaltered. Intrinsic excitatory connections remain functional; this is also true for the disynaptic inhibitory pathways activated preferentially by the fast-conducting thalamocortical projection. The laminar distribution of cells with monosynaptic versus polsynaptic excitatory connections is similar to that in normal cats. Neurons with corticofugal axons remain functionally connected and show the same connectivity pattern as those in normal cats. The nonspecific activation system from the mesencephalic reticular formation also remains functioning both at the thalamic and the cortical level.We conclude from these and several other observations that most, if not all, afferent, intrinsic, and efferent connections of areas 17 and 18 are specified from birth and depend only little on visual experience. This predetermined structural plan, however, allows for some freedom in the domain of orientation tuning, binocular correspondence, and retinotopy which is specified only when visual experience is possible.

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Distributed spatial coding in the superior colliculus: A review

Visual Neuroscience ◽

10.1017/s0952523800000857 ◽

1991 ◽

Vol 6 (1) ◽

pp. 3-13 ◽

Cited By ~ 60

Author(s):

James T. McIlwain

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Receptive Fields ◽

Saccadic Eye Movements ◽

Visual Direction ◽

Saccade Amplitude ◽

Spatial Coding ◽

Distributed Coding

AbstractThis paper reviews evidence that the superior colliculus (SC) of the midbrain represents visual direction and certain aspects of saccadic eye movements in the distribution of activity across a population of cells. Accurate and precise eye movements appear to be mediated, in part at least, by cells of the SC that have large sensory receptive fields and/or discharge in association with a range of saccades. This implies that visual points or saccade targets are represented by patches rather than points of activity in the SC. Perturbation of the pattern of collicular discharge by focal inactivation modifies saccade amplitude and direction in a way consistent with distributed coding. Several models have been advanced to explain how such a code might be implemented in the colliculus. Evidence related to these hypotheses is examined and continuing uncertainties are identified.

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Context dependence of receptive field remapping in superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.00288.2011 ◽

2011 ◽

Vol 106 (4) ◽

pp. 1862-1874 ◽

Cited By ~ 20

Author(s):

Jan Churan ◽

Daniel Guitton ◽

Christopher C. Pack

Keyword(s):

Receptive Field ◽

Superior Colliculus ◽

Visual Stimulation ◽

Receptive Fields ◽

Spatial Location ◽

Macaque Monkey ◽

Visual Signals ◽

Perceptual Stability ◽

Visual Background ◽

The Brain

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.

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